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Adaptation: From single cells to BOLD signals
Abstract
Functional magnetic resonance imaging adaptation (fMRIa) is an increasingly popular method that aims to provide insight into the functional properties of subpopulations of neurons within an imaging voxel. The technique relies on the assumption that neural adaptation reduces activity when two successive stimuli activate the same subpopulation but not when they stimulate different subpopulations. Here, we assess the validity of fMRIa by comparing single-cell recordings with functional imaging of orientation, motion and face processing. We find that fMRIa provides novel insight into neural representations in the human brain. However, network responses in general and adaptation in particular are more complex than is often assumed, and an unequivocal interpretation of fMRIa results can be achieved only with great care.
... At re-test, patients with overly 24 steep slopes in the narrow range also showed higher levels of negative symptoms. 25 Our data confirm deficits in reward adaptation in schizophrenia and reveal a practice effect in 26 patients, leading to improvement, with steeper slopes upon retest. However, in some patients, an 27 A C C E P T E D M A N U S C R I P T ownloaded from https://academic.oup.com/brain/advance-article/doi/10.1093/brain/awae112/7644964 by Forschungsstelle fuer schweizerische Sozialund Wirtschaftsgeschichte der Universitaet Zuerich user on 25 April 2024 Introduction 22 In order to adequately represent the rewarding value of everyday actions and events, the brain 23 needs to adapt to the context of available rewards. ...
... You can be perfectly happy with your salary 24 until you learn your colleague is earning more. Adaptation is driven by our neuronal systems 25 A C C E P T E D M A N U S C R I P T Previous work has indeed shown an association between deficient adaptive coding of the reward 23 range predicted by conditioned stimuli and negative symptoms in schizophrenia. At the neural 24 level, adaptive coding in the striatum and the precentral gyrus inversely related to the psychosis 25 spectrum, strongest in healthy participants with high schizotypy scores, intermediate in first 26 episode psychosis and weakest in patients with chronic schizophrenia 9 . ...
... Adaptation is driven by our neuronal systems 25 A C C E P T E D M A N U S C R I P T Previous work has indeed shown an association between deficient adaptive coding of the reward 23 range predicted by conditioned stimuli and negative symptoms in schizophrenia. At the neural 24 level, adaptive coding in the striatum and the precentral gyrus inversely related to the psychosis 25 spectrum, strongest in healthy participants with high schizotypy scores, intermediate in first 26 episode psychosis and weakest in patients with chronic schizophrenia 9 . Moreover, the reduction 27 in reward adaptation correlated with negative, positive and global symptom severity (as measured 28 by the PANSS) 8,9 . ...
Adaptive coding of reward is the process by which neurons adapt their response to the context of available compensations. Higher rewards lead to a stronger brain response, but the increase of the response depends on the range of available rewards. A steeper increase is observed in a narrow range, and a more gradual slope in a wider range. In schizophrenia, adaptive coding appears affected in different domains, and in the reward domain in particular. Here we tested adaptive coding of reward in a large group of patients with schizophrenia (N = 86) and controls (N = 66). We assessed 1) the association between adaptive coding deficits and symptoms; 2) the longitudinal stability of deficits (the same task was performed three months apart); 3) the stability of results between two experimental sites.
We used fMRI and the Monetary Incentive Delay task to assess participant’ adaptation to two different reward ranges: a narrow and a wide range. We used a region of interest analysis, evaluating adaptation within striatal and visual regions. Patients and controls underwent a full demographic and clinical assessment.
We found reduced adaptive coding in patients, due to a decreased slope in the narrow reward range, with respect to that of control participants in striatal but not visual regions. This pattern was observed at both research sites. Upon re-test, patients increased their narrow range slopes, showing improved adaptive coding, whereas controls slightly reduced them. At re-test, patients with overly steep slopes in the narrow range also showed higher levels of negative symptoms.
Our data confirm deficits in reward adaptation in schizophrenia and reveal a practice effect in patients, leading to improvement, with steeper slopes upon retest. However, in some patients, an overly steep slope may result in poor discriminability of larger rewards, due to early saturation of the brain response. Together, the loss of precision of reward representation in new (first exposure, underadaptation) and more familiar (re-test, overadaptation) situations may contribute to the multiple motivational symptoms in schizophrenia.
... Functional magnetic resonance imaging (fMRI)-based adaptation has been used to infer stimulus selectivity by response reduction, defining repetition suppression. This technique became a popular method to study the selectivity of populations of neurons related to orientation, motion, and face processing in humans (Krekelberg et al., 2006). However, the need for a better understanding of the relationship between the stimulus selectivity of neuronal adaptation and responses has been pointed out (Sawamura et al., 2006). ...
... It is important to point out that testing conflicting opposite local directions often leads to response reduction but not perceptual oscillations (a distinct phenomenon known as motion opponency). The response to opponent motion in MT neurons might lead to an average response that is similar to the average response of the neuron to both the preferred and non-preferred directions (Krekelberg et al., 2006;Krekelberg and van Wezel, 2013;Silva et al., 2021). However, fluctuations in the response to opponent motion and their relation to changes in perception remain unknown. ...
... adaptation). Neuronal adaptation, also known as repetition suppression, is known to result from repeated stimulation and to lead to a smaller amplitude of the measured neurophysiological signal (Grill-Spector and Malach, 2001;Krekelberg et al., 2006;Tootell et al., 1998). In a previous study, we found that during moving plaid visualization, visual adaptation was stronger upon coherent and into a lesser extent, incoherent percepts (Sousa et al., 2018). ...
... This technique became a popular method to show selectivity of populations of neurons. Its validity was demonstrated by comparing single-cell recordings with functional imaging of orientation, motion, and face processing (5), which showed remarkable consistency across experimental models. ...
... The hMT+/V5 responses were initially lower than during non-adapting conditions and this effect was stronger during the adaptation to coherent motion pattern (the expected difference induced by adaptation). Neuronal adaptation, also known as repetition suppression, is known to result from repeated stimulation and to lead to a smaller amplitude of the measured neurophysiological signal (5,47,48). In a previous study, we found that during moving plaid visualization, visual adaptation was stronger upon coherent and into a lesser extent, incoherent percepts (45). ...
A model based on inhibitory coupling has been proposed to explain perceptual oscillations. This ‘adapting reciprocal inhibition’ model postulates that it is the strength of inhibitory coupling that determines the fate of competition between percepts. Here, we used an fMRI-based adaptation technique to reveal the influence of neighboring neuronal populations, such as reciprocal inhibition, in motion-selective hMT+/V5. If reciprocal inhibition exists in this region, the following predictions should hold: 1. stimulus-driven response would not simply decrease, as predicted by simple repetition-suppression of neuronal populations, but instead increase due to the activity from adjacent populations; 2. perceptual decision involving competing representations, should reflect decreased reciprocal inhibition by adaptation; 3. neural activity for the competing percept should also later on increase upon adaptation. Our results confirm these three predictions, showing that a model of perceptual decision based on adapting reciprocal inhibition holds true. Finally, they also show that the well-known repetition suppression phenomenon can be reversed by this mechanism.
Significance Statement
fMRI-based adaptation has been developed as a tool to identify functional selectivity in the human brain. This is based on the notion that stimulus-selective adaptation leads to direct response suppression. In this study, we go a step further by showing that adaptation can also reveal the influence of neighboring neuronal populations. Our data reveals neural evidence for a disinhibition effect as a result of the adaptation of adjacent populations, which is in line with the adapting reciprocal inhibition model. Reciprocal inhibition can, thus, be tracked in the human brain using fMRI, adding to the understanding of human multistable perception and the neural coding of visual information. Moreover, our results also provide a mechanism for reversal of repetition suppression.
... Sensory adaptation has been shown to relate to reduction in 1) neuronal responses to the features of the adaptor, as measured by electrophysiology (for review Kohn 2007) and 2) blood oxygen level-dependent (BOLD) responses to low-level features (e.g., contrast, orientation, motion; for review Larsson et al. 2016) in visual cortex due to stimulus repetition, as measured by functional brain imaging. Further, repetition suppression (i.e., decreased BOLD for repeated stimuli) has been reported in higher visual areas for repeated presentation of more complex visual stimuli (e.g., faces, objects) (Grill-Spector et al. 2006;Krekelberg et al. 2006). In contrast, repetition enhancement (i.e., increased BOLD for repeated compared to novel stimuli) has been reported in parietal, temporal, and frontal regions known to be involved in memory rather than sensory processes (for review Segaert et al. 2013). ...
... First, we show repetition suppression (i.e., decreased fMRI responses) in visual cortex and dlPFC, consistent with previous studies showing decreased fMRI and neuronal responses for orientation-specific adaptation in visual cortex (Clifford 2002;Krekelberg et al. 2006) and the role of dlPFC in processing and monitoring familiar stimuli (Henson et al. 1999;Petrides 2005;Kim 2011). Further, we show increased functional connectivity between primary visual cortex (V1) and posterior parietal cortex (i.e., IPS) for familiar stimuli. ...
The brain’s capacity to adapt to sensory inputs is key for processing sensory information efficiently and interacting in new environments. Following repeated exposure to the same sensory input, brain activity in sensory areas is known to decrease as inputs become familiar, a process known as adaptation. Yet, the brain-wide mechanisms that mediate adaptive processing remain largely unknown. Here, we combine multimodal brain imaging (functional magnetic resonance imaging [fMRI], magnetic resonance spectroscopy) with behavioral measures of orientation-specific adaptation (i.e., tilt aftereffect) to investigate the functional and neurochemical mechanisms that support adaptive processing. Our results reveal two functional brain networks: 1) a sensory-adaptation network including occipital and dorsolateral prefrontal cortex regions that show decreased fMRI responses for repeated stimuli and 2) a perceptual-memory network including regions in the parietal memory network (PMN) and dorsomedial prefrontal cortex that relate to perceptual bias (i.e., tilt aftereffect). We demonstrate that adaptation relates to increased occipito-parietal connectivity, while decreased connectivity between sensory-adaptation and perceptual-memory networks relates to GABAergic inhibition in the PMN. Thus, our findings provide evidence that suppressive interactions between sensory-adaptation (i.e., occipito-parietal) and perceptual-memory (i.e., PMN) networks support adaptive processing and behavior, proposing a key role of memory systems in efficient sensory processing.
... The specificity of neural representations has often been investigated with adaptation paradigms. A neural population, which encodes a specific feature of a stimulus, decreases its activity when this feature remains constant across repeated presentations, but increases it again when this feature changes [70][71][72]. Repetition suppression in response to a repeated presentation of sound objects has been documented by electrophysiological recordings as a decrease in evoked potential amplitude and shown to occur within a critical time window post-stimulus onset [73,74]. ...
Auditory spatial cues contribute to two distinct functions, of which one leads to explicit localization of sound sources and the other provides a location-linked representation of sound objects. Behavioral and imaging studies demonstrated right-hemispheric dominance for explicit sound localization. An early clinical case study documented the dissociation between the explicit sound localizations, which was heavily impaired, and fully preserved use of spatial cues for sound object segregation. The latter involves location-linked encoding of sound objects. We review here evidence pertaining to brain regions involved in location-linked representation of sound objects. Auditory evoked potential (AEP) and functional magnetic resonance imaging (fMRI) studies investigated this aspect by comparing encoding of individual sound objects, which changed their locations or remained stationary. Systematic search identified 1 AEP and 12 fMRI studies. Together with studies of anatomical correlates of impaired of spatial-cue-based sound object segregation after focal brain lesions, the present evidence indicates that the location-linked representation of sound objects involves strongly the left hemisphere and to a lesser degree the right hemisphere. Location-linked encoding of sound objects is present in several early-stage auditory areas and in the specialized temporal voice area. In these regions, emotional valence benefits from location-linked encoding as well.
... In neuroscience research, visual adaptation has been documented through psychophysical experiments [6,7] and electrophysiological recordings [8,9]. In functional imaging, adaptation serves as a signature of region-specific encoding, with regions responsive to a specific feature displaying reduced activity [10][11][12][13]. Conversely, the search for a neural correlate of the MAE focused on increased activity in non-adapted neuron populations [14,15]. ...
Adaptation is a form of short-term plasticity triggered by prolonged exposure to a stimulus, often resulting in altered perceptual sensitivity to stimulus features through a reduction in neuronal firing rates. Experimental studies have explored adaptation to bistable stimuli, specifically a stimulus comprising inward-moving plaids that can be perceived as either a grating moving coherently downward or two plaids moving incoherently through each other. Functional magnetic resonance imaging (fMRI) recordings have shown higher activity during incoherent perception and lower activity during coherent stimulus perception. There are two potential explanations for the underlying neural mechanisms: a weaker coherent stimulus response may result from stronger adaptation to coherent versus incoherent motion, or a stronger incoherent stimulus response could stem from the involvement of more neural populations to represent motion in more directions. Here, we employ a computational model of visual neurons with and without firing rate adaptation to test these hypotheses. By simulating the mean activity of a network of thirty-two columnar populations of visual area MT, each tuned to one direction of motion, we investigate the impact of firing rate adaptation on the blood-oxygen-level-dependent (BOLD) signal generated by the network in response to coherent and incoherent stimuli. Our results replicate the experimental curves both during and after stimulus presentation only when the model includes adaptation, highlighting the importance of this mechanism. However, our findings reveal that the response to incoherent motion is larger than the response to coherent motion for a wide variety of stimulus parameters and adaptation regimes, suggesting that the observed reduced response to coherent stimuli is most likely due to the activation of smaller neuronal populations, in alignment with the second hypothesis. Hence, adaptation and differential neuronal recruitment work together to give rise to the observed hemodynamic responses. This computational work sheds light on experimental results and enriches our understanding of the mechanisms involved in neural adaptation, particularly in the context of heterogeneous neuronal populations.
... The first analytical approach that we implemented was a univariate adaptation analysis, building on the observation that the fMRI BOLD signal shows suppression (or adapts) when stimuli are repeated, potentially because of the adaptation of the underlying neuronal populations 59,60 . We reasoned that if a brain region is representing specific egocentric conditions differently, then it should show a suppression pattern specific to each individual condition. ...
The human hippocampal-entorhinal system is known to represent both spatial locations and abstract concepts in memory in the form of allocentric cognitive maps. Using fMRI, we show that the human parietal cortex evokes complementary egocentric representations in conceptual spaces during goal-directed mental search, akin to those observable during physical navigation to determine where a goal is located relative to oneself (e.g., to our left or to our right). Concurrently, the strength of the grid-like signal, a neural signature of allocentric cognitive maps in entorhinal, prefrontal, and parietal cortices, is modulated as a function of goal proximity in conceptual space. These brain mechanisms might support flexible and parallel readout of where target conceptual information is stored in memory, capitalizing on complementary reference frames.
... Besides the ongoing debate on whether repetition suppression can accurately infer neural selectivity and the precise nature of the neuronal mechanisms underlying repetition suppression [9][10][11][12][13][14], there are currently limited data regarding possible uni-modal or crossmodal adaptation effects at the single-cell or population level in monkey mirror neuron regions [15,16]. Previous work from our lab has shown uni-modal visual fMRI adaptation effects in early visual cortices but did not find uni-or cross-modal fMRI adaptation effects in monkey parietal and premotor mirror neuron regions [2]. ...
To probe the presence of mirror neurons in the human brain, cross-modal fMRI adaptation has been suggested as a suitable technique. The rationale behind this suggestion is that this technique allows making more accurate inferences about neural response properties underlying fMRI voxel activations, beyond merely showing shared voxels that are active during both action observation and execution. However, the validity of using cross-modal fMRI adaptation to demonstrate the presence of mirror neurons in parietal and premotor brain regions has been questioned given the inconsistent and weak results obtained in human studies. A better understanding of cross-modal fMRI adaptation effects in the macaque brain is required as the rationale for using this approach is based on several assumptions related to macaque mirror neuron response properties that still need validation. Here, we conducted a cross-modal fMRI adaptation study in macaque monkeys, using the same action execution and action observation tasks that successfully yielded mirror neuron region cross-modal action decoding in a previous monkey MVPA study. We scanned two male rhesus monkeys while they first executed a sequence of either reach-and-grasp or reach-and-touch hand actions and then observed a video of a human actor performing these motor acts. Both whole-brain and region-of-interest analyses failed to demonstrate cross-modal fMRI adaptation effects in parietal and premotor mirror neuron regions. Our results, in line with previous findings in non-human primates, show that cross-modal motor-to-visual fMRI adaptation is not easily detected in monkey brain regions known to house mirror neurons. Thus, our results advocate caution in using cross-modal fMRI adaptation as a method to infer whether mirror neurons can be found in the primate brain.
... These aftereffects arise, in part, due to attenuation in the responses of neurons that code the 317 features of the prior stimulus(feature-specific adaptation), which then biases the population 318 response to subsequent stimuli away from the adapted features (50)(51)(52). There is growing 319 evidence from the basic cognitive literature that serial dependence in WM reflects a mixture of 320 J o u r n a l P r e -p r o o f 14 repulsion arising from this sort of neuronal adaptation with attraction arising from STP or some 321 other mechanism (53,54). ...
Background:
Impairments in working memory(WM) have been well-documented in people with schizophrenia(PSZ). However, these quantitative WM impairments can often be explained by nonspecific factors, such as impaired goal maintenance. Here, we used a spatial orientation delayed-response task to explore a qualitative difference in WM dynamics between PSZ and healthy control subjects(HCS). Specifically, we took advantage of the discovery that WM representations may drift either toward or away from previous-trial targets(serial dependence). We tested the hypothesis that WM representations drift toward the previous-trial target in HCS but away from the previous-trial target in PSZ.
Methods:
We assessed serial dependence in PSZ(N=31) and HCS(N=25), using orientation as the to-be-remembered feature and memory delays from 0 to 8s. Participants were asked to remember the orientation of a teardrop-shaped object and reproduce the orientation after a varying delay period.
Results:
Consistent with prior studies, we found that current-trial memory representations were less precise in PSZ than in HCS. We also found that WM for the current-trial orientation drifted toward the previous-trial orientation in HCS(representational attraction) but drifted away from the previous-trial orientation in PSZ(representational repulsion).
Conclusions:
These results demonstrate a qualitative difference in WM dynamics between PSZ and HCS that cannot easily be explained by nuisance factors such as reduced effort. Most computational neuroscience models also fail to explain these results, because they maintain information solely by means of sustained neural firing, which does not extend across trials. The results suggest a fundamental difference between PSZ and HCS in longer-term memory mechanisms that persist across trials, such as short-term potentiation and neuronal adaptation.
... This limits our ability to directly compare findings in non-visual areas to the visual system, which is most responsive to the stimuli. Additionally, while neural-BOLD adaptation to repeated visual stimuli has been well-observed in the visual cortex (Grill-Spector et al., 2006;Krekelberg et al., 2006), it is unclear how it contributes to QPPs among all brain regions. Although we did not investigate BOLD adaptation in the current study, any changes in QPPs due to neural adaptation would be reflected in the overall pattern of QPP, which is an averaged pattern across all concatenated runs. ...
One prominent feature of the infraslow BOLD signal during rest or task is quasi-periodic spatiotemporal pattern (QPP) of signal changes that involves an alternation of activity in key functional networks and propagation of activity across brain areas, and that is known to tie to the infraslow neural activity involved in attention and arousal fluctuations. This ongoing whole-brain pattern of activity might potentially modify the response to incoming stimuli or be modified itself by the induced neural activity. To investigate this, we presented checkerboard sequences flashing at 6Hz to subjects. This is a salient visual stimulus that is known to produce a strong response in visual processing regions. Two different visual stimulation sequences were employed, a systematic stimulation sequence in which the visual stimulus appeared every 20.3 secs and a random stimulation sequence in which the visual stimulus occurred randomly every 14∼62.3 secs. Three central observations emerged. First, the two different stimulation conditions affect the QPP waveform in different aspects, i.e., systematic stimulation has greater effects on its phase and random stimulation has greater effects on its magnitude. Second, the QPP was more frequent in the systematic condition with significantly shorter intervals between consecutive QPPs compared to the random condition. Third, the BOLD signal response to the visual stimulus across both conditions was swamped by the QPP at the stimulus onset. These results provide novel insights into the relationship between intrinsic patterns and stimulated brain activity.
... These aftereffects arise, in part, due to attenuation in the responses of neurons that code the 300 features of the prior stimulus (feature-specific adaptation), which then biases the population 301 response to subsequent stimuli away from the adapted features (50)(51)(52). There is growing 302 evidence from the basic cognitive literature that serial dependence in WM reflects a mixture of 303 repulsion arising from this sort of neuronal adaptation with attraction arising from STP or some 304 other mechanism (53,54). ...
Background
Impairments in working memory(WM) have been well-documented in people with schizophrenia(PSZ). However, these quantitative WM impairments can often be explained by nonspecific factors, such as impaired goal maintenance. Here, we used a spatial orientation delayed-response task to explore a qualitative difference in WM dynamics between PSZ and healthy control subjects(HCS). Specifically, we took advantage of the discovery that WM representations may drift either toward or away from previous-trial targets(serial dependence). We tested the hypothesis that WM representations drift toward the previous-trial target in HCS but away from the previous-trial target in PSZ.
Methods
We assessed serial dependence in PSZ(N=31) and HCS(N=25), using orientation as the to-be-remembered feature and memory delays from 0 to 8s. Participants were asked to remember the orientation of a teardrop-shaped object and reproduce the orientation after a varying delay period.
Results
Consistent with prior studies, we found that current-trial memory representations were less precise in PSZ than in HCS. We also found that WM for the current-trial orientation drifted toward the previous-trial orientation in HCS(representational attraction) but drifted away from the previous-trial orientation in PSZ(representational repulsion).
Conclusions
These results demonstrate a qualitative difference in WM dynamics between PSZ and HCS that cannot easily be explained by nuisance factors such as reduced effort. Most computational neuroscience models also fail to explain these results, because they maintain information solely by means of sustained neural firing, which does not extend across trials. The results suggest a fundamental difference between PSZ and HCS in longer-term memory mechanisms that persist across trials, such as short-term potentiation and neuronal adaptation.
... In addition, we assessed the linearity or nonlinearity of the HDRs induced by increasing stimulation durations in the primary auditory cortex. This analysis aims to improve the design of fNIRS auditory experiments when task duration varies (Soltysik et al., 2004) and to increase the understanding of brain adaptation peculiarities (Krekelberg et al., 2006) . ...
Introduction La surdité unilatérale est une pathologie fréquente chez l'enfant. Les répercussions en sont importantes tant sur le plan de l'audition spatiale que sur l'aspect du développement psychosocial. À ce jour, très peu de données neurofonctionnelles ont été recueillies chez l'enfant. L'objectif de cette thèse est donc d'étudier, chez l'enfant, le lien entre l'atteinte auditive unilatérale et ses corrélats neuraux. Cet objectif repose sur deux études, lesquelles sont définies comme suit : 1) Procéder à l'identification des paramètres de stimulation optimaux utilisés en fNIRS afin d'obtenir un signal de qualité sur l'enfant et, 2) Mesurer la réorganisation corticale suite à la surdité unilatérale et corréler cette réorganisation aux performances psychoacoustiques, psychosociales. Matériels et méthodes S'agissant de la première étude, dix-sept sujets adultes normo-entendants ont été recrutés. Ils ont été soumis à quatre conditions de stimulation auditive en fNIRS. L'amplitude du signal fNIRS enregistré et la durée expérimentale ont été comparées, entre ces conditions. Concernant la seconde étude, quatre enfants porteurs de surdité unilatérale ont été inclus. Ils ont été évalués en psychoacoustique par les tests de localisation du son dans l'espace et de la compréhension de la parole dans le bruit, en neurofonctionnel par la fNIRS, et en développement psychosocial par les tests mesurant les habiletés linguistiques différentes. Ils ont enfin répondu aux questionnaires de qualité de vie. Résultats L'étude 1 a identifié la durée de stimulation de 15 s comme étant un choix optimal, lorsqu'elle est associée à une amplitude trois fois plus importante et à une durée plus courte de 105 s que les autres conditions de stimulation. L'étude 2 a démontré une grande variabilité des résultats en performances psychoacoustiques et psychosociales. De plus, la surdité unilatérale a induit une augmentation de l'activation corticale ipsilatérale à l'oreille saine. Cette augmentation est significativement corrélée aux performances binaurales. Conclusion La surdité unilatérale induit des phénomènes de réorganisation corticale associés à une forte variabilité des performances binaurales et psychosociales, suggérant l'existence de facteurs compensatoires. Ce travail souligne la nécessité de l'identification de ces facteurs compensatoires et d'une prise en charge des enfants vulnérables aux effets néfastes de la surdité unilatérale.
... Values greater than 0.95 are taken as strong evidence (shown in bold emphasis). connections in the right hemisphere suggest that local changes within EVC (e.g., fatigue or sharpening) are not sufficient to explain "downstream " RS in OFA and FFA (or "inherited adaptation ", Krekelberg et al., 2006 ). Further implications of these results are considered in the Discussion, after comparing with results from the final 6-ROI network. ...
Stimulus repetition normally causes reduced neural activity in brain regions that process that stimulus. Some theories claim that this “repetition suppression” reflects local mechanisms such as neuronal fatigue or sharpening within a region, whereas other theories claim that it results from changed connectivity between regions, following changes in synchrony or top-down predictions. In this study, we applied dynamic causal modelling (DCM) on a public fMRI dataset involving repeated presentations of faces and scrambled faces to test whether repetition affected local (self-connections) and/or between-region connectivity in left and right early visual cortex (EVC), occipital face area (OFA) and fusiform face area (FFA). Face “perception” (faces versus scrambled faces) modulated nearly all connections, within and between regions, including direct connections from EVC to FFA, supporting a non-hierarchical view of face processing. Face “recognition” (familiar versus unfamiliar faces) modulated connections between EVC and OFA/FFA, particularly in the left hemisphere. Most importantly, immediate and delayed repetition of stimuli were also best captured by modulations of connections between EVC and OFA/FFA, but not self-connections of OFA/FFA, consistent with synchronization or predictive coding theories, though also possibly reflecting local mechanisms like synaptic depression.
... One way the visual system does this is by adaptation (Hosoya et al., 2005;Lan et al., 2012;Laughlin, 1989;Sharpee et al., 2006). Visual adaptation is a mechanism by which the sensitivity of a neuron (or neural network) adjusts its firing rate depending on the exposure duration of a stimulus (for reviews from varying perspectives, see Clifford et al., 2007;Kohn, 2007;Krekelberg et al., 2006;Rieke & Rudd, 2009;Webster, 2015): most neurons are less likely to fire as stimulus presentation time within their receptive fields increases. Adaptation further strengthens when the stimulus targets exactly the feature that a neuron or neural population "prefers," that is right at the center of their tuning curve (Clifford, 2002;Clifford et al., 2007). ...
The eye’s retinotopic exposure to an adapter typically produces an after-image. For example, an observer who fixates a red adapter on a gray background will see an illusory cyan after-image after removing the adapter. The after-image’s content, like its color or intensity, gives insight into mechanisms responsible for adaptation and processing of a specific feature. To facilitate adaptation, vision scientists traditionally present stable, unchanging adapters for prolonged durations. How adaptation affects perception when features (e.g., color) dynamically change over time is not understood. To investigate adaptation to a dynamically changing feature, participants viewed a colored patch that changed from a color to gray, following either a direct or curved path through the (roughly) equiluminant color plane of CIE LAB space. We varied the speed and curvature of color changes across trials and experiments. Results showed that dynamic adapters produce after-images, vivid enough to be reported by the majority of participants. An after-image consisted of a color complementary to the average of the adapter’s colors with a small bias towards more recent rather than initial adapter colors. The modelling of the reported after-image colors further confirmed that adaptation rapidly instigates and gradually dissipates. A second experiment replicated these results and further showed that the probability of observing an after-image diminishes only slightly when the adapter displays transient (stepwise, abrupt) color transitions. We conclude from the results that the visual system can adapt to dynamic colors, to a degree that is robust to the potential interference of transient changes in adapter content.
... Since the ERP difference between the effects of the deviant and standard stimuli could be the result of either a decrease in activity in response to the standards (Krekelberg et al., 2006;May and Tiitinen, 2010;May, 2021) or additional activity elicited by the deviants (Kimura et al., 2011;Stefanics et al., 2014), an important limitation of the current study is the lack of control sequences. The initial reasoning for not applying control sequences was based on the physical differences between marginal and central interest changes, that is, the areas of the marginal changes (mean difference = 22 square degree) were somewhat larger than the those of central changes (mean difference = 18 square degree) (Rensink et al., 1997). ...
Change blindness experiments had demonstrated that detection of significant changes in natural images is extremely difficult when brief blank fields are placed between alternating displays of an original and a modified scene. On the other hand, research on the visual mismatch negativity (vMMN) component of the event-related potentials (ERPs) identified sensitivity to events (deviants) different from the regularity of stimulus sequences (standards), even if the deviant and standard events are non-attended. The present study sought to investigate the apparent controversy between the experience under the change blindness paradigm and the ERP results. To this end, the stimulus of Rensink, O’Reagen, and Clark (1997) was adapted to a passive oddball ERP paradigm to investigate the underlying processing differences between the standard (original) and deviant (altered) stimuli measured in 22 subjects. Posterior negativity within the 280–330 ms latency range emerged as the difference between ERPs elicited by standard and deviant stimuli, identified as visual mismatch negativity (vMMN). These results raise the possibility that change blindness is not based on the lack of detailed visual representations or the deficiency of comparing two representations. However, effective discrimination of the two scene versions requires considerable frequency differences between them.
... In humans, advances have been made by using brain stimulation techniques to target regions identified by functional imaging (Pitcher et al., 2007;Sliwinska and Pitcher, 2018), and by event-related potentials, sometimes in combination with functional imaging (Sadeh et al., 2010;Dalrymple et al., 2011), to help us understand the specific roles played by different face-selective areas. Similarly, adaptation techniques in functional imaging (Grill-Spector and Malach, 2001;Krekelberg et al., 2006) have allowed us to ask not just whether an area is activated by faces, but what type of facial properties are reflected in its signal. ...
Face perception is a socially important but complex process with many stages and many facets. There is substantial evidence from many sources that it involves a large extent of the temporal lobe, from the ventral occipitotemporal cortex and superior temporal sulci to anterior temporal regions. While early human neuroimaging work suggested a core face network consisting of the occipital face area, fusiform face area, and posterior superior temporal sulcus, studies in both humans and monkeys show a system of face patches stretching from posterior to anterior in both the superior temporal sulcus and inferotemporal cortex. Sophisticated techniques such as fMRI adaptation have shown that these face-activated regions show responses that have many of the attributes of human face processing. Lesions of some of these regions in humans lead to variants of prosopagnosia, the inability to recognize the identity of a face. Lesion, imaging, and electrophysiologic data all suggest that there is a segregation between identity and expression processing, though some suggest this may be better characterized as a distinction between static and dynamic facial information.
... Guided interpretable designs, including model architecture, objective function and learning algorithm, in the spirit of explainable AI will be key in modeling brain data using end-to-end deep learning models of information encoding. Key principles of neural computation known from previous work may need to be incorporated in the architectures of these models, including hierarchical processing with integrated local and feedback recurrence loops [96,97], neural adaptation [98,99,100], sparse coding principles [101], temporal stability for noise robustness and code invariance [102,103,104], stochasticity in neural signals [105,106] and oscillatory dynamics [107,108]. However, given that detailed workings of many of these principles remain debated in neuroscience, end-to-end DNN encoding models could also provide an excellent framework for testing associated theory-driven hypotheses in silico [72]. ...
Artificial intelligence (AI) is a fast-growing field focused on modeling and machine implementation of various cognitive functions with an increasing number of applications in computer vision, text processing, robotics, neurotechnology, bio-inspired computing and others. In this chapter, we describe how AI methods can be applied in the context of intracranial electroencephalography (iEEG) research. IEEG data is unique as it provides extremely high-quality signals recorded directly from brain tissue. Applying advanced AI models to these data carries the potential to further our understanding of many fundamental questions in neuroscience. At the same time, as an invasive technique, iEEG lends itself well to long-term, mobile brain-computer interface applications, particularly for communication in severely paralyzed individuals. We provide a detailed overview of these two research directions in the application of AI techniques to iEEG. That is, (1) the development of computational models that target fundamental questions about the neurobiological nature of cognition (AI-iEEG for neuroscience) and (2) applied research on monitoring and identification of event-driven brain states for the development of clinical brain-computer interface systems (AI-iEEG for neurotechnology). We explain key machine learning concepts, specifics of processing and modeling iEEG data and details of state-of-the-art iEEG-based neurotechnology and brain-computer interfaces.
... To this aim, we used a functional magnetic resonance adaptation (fMRI-A) paradigm, presenting words pairs belonging to different concrete and abstract categories in a passive reading task. fMRI-A allows the exploration of the functional properties of a neural population, making use of the property displayed by some neurons of reducing their response to a repeatedly presented stimulus 29,30 . The underlying assumption is that, if the brain area remains adapted to the second stimulus, this indicates that its neural population is coding the attributes shared between the two stimuli 31 . ...
Concrete conceptual knowledge is supported by a distributed neural network representing different semantic features according to the neuroanatomy of sensory and motor systems. If and how this framework applies to abstract knowledge is currently debated. Here we investigated the specific brain correlates of different abstract categories. After a systematic a priori selection of brain regions involved in semantic cognition, i.e. responsible of, respectively, semantic representations and cognitive control, we used a fMRI-adaptation paradigm with a passive reading task, in order to modulate the neural response to abstract (emotions, cognitions, attitudes, human actions) and concrete (biological entities, artefacts) categories. Different portions of the left anterior temporal lobe responded selectively to abstract and concrete concepts. Emotions and attitudes adapted the left middle temporal gyrus, whereas concrete items adapted the left fusiform gyrus. Our results suggest that, similarly to concrete concepts, some categories of abstract knowledge have specific brain correlates corresponding to the prevalent semantic dimensions involved in their representation.
... In order to answer this question we used fMRI adaptation 23,24 , an approach previously employed to detect the neural representation of faced direction during spatial tasks in virtual environments (e.g., refs. 5,11,14 ). ...
When humans mentally “navigate” bidimensional uniform conceptual spaces, they recruit the same grid-like and distance codes typically evoked when exploring the physical environment. Here, using fMRI, we show evidence that conceptual navigation also elicits another kind of spatial code: that of absolute direction. This code is mostly localized in the medial parietal cortex, where its strength predicts participants’ comparative semantic judgments. It may provide a complementary mechanism for conceptual navigation outside the hippocampal formation.
... Adaptation can occur at different levels according to the depth of cognitive processing (Webster, 2011;Webster & MacLeod, 2011). Low-level adaptation has been found for the processing of color, orientation, and direction of motion (Krekelberg et al., 2006;Kuriki, 2007;Thompson & Burr, 2009;Tskhay & Rule, 2015). At a higher cognitive level, adaptation has been reported for aspect ratio (Suzuki & Cavanagh, 1998), three-dimensional viewpoint (Fang & He, 2005), surface reflectance (Goddard et al., 2010), and words and objects (Perrachione et al., 2016;Reindl et al., 2018). ...
The adaptation aftereffect plays a critical role in human development and survival. Existing studies have found that, compared with general individuals, individuals with learning disability, autism and dyslexia show a smaller amount of non-affective-based cognitive adaptation aftereffect. Nevertheless, it is unclear whether individuals with depression or depression tendency show similar phenomenon in the adaptation aftereffect, and whether such depression tendency occurs in the non-affective-based cognitive or emotional adaptation aftereffect. To address this question, the present study conducted two experiments. Experiments 1A and 1B used the emotional facial expression adaptation paradigm to examine whether Chinese participants showed the emotional adaptation aftereffect and whether the emotional adaptation aftereffect was influenced by physical features of faces, respectively. Experiment 2 recruited two groups of participants, with high and low depression, respectively, to examine whether they showed differences in the emotional or cognitive adaptation aftereffect. Results showed that Chinese participants showed the typical emotional adaptation aftereffect, which was not influenced by physical features of faces. More importantly, compared to the low-depression group, the high-depression group showed a smaller emotional adaptation aftereffect, but the two groups showed a similar cognitive adaptation aftereffect. These results suggest that level of depressive symptoms is associated with the emotional adaptation aftereffect.
... Selective adaptation is the process by which prolonged exposure to a stimulus causes desensitization of cortical neurons, resulting in perceptual changes (Goldstein and Brockmole, 2016;Snowden et al., 2012). Adaptation is critical for efficient neural coding, and its effects have been well characterized at the psychological and neural levels (for review, see Clifford, 2002;Krekelberg et al., 2006;Webster, 2011). Adaptation aftereffects are ubiquitous in the sensory domain and lead to marked biases in perception. ...
Prolonged exposure to a stimulus causes desensitization of cortical neurons and results in perceptual changes. One example of this phenomenon is contrast adaptation, in which perceived differences between light and dark regions of a stimulus decrease. Blakemore, Muncey, and Ridley reported evidence for the "perceptual fading of a stabilized cortical image" in a 1971 Nature paper. Our goal was to replicate their second experiment, in which adaptation was measured across many contrasts, and develop an active learning exercise for undergraduate students. The experiment was coded using an open-source python package and psychophysical data were collected from two observers. On each trial, a sinusoidally modulated luminance grating appeared above fixation, and the task of the observer was to adjust the contrast of a grating below fixation until the two appeared identical. Between trials in the adaptation condition, a high contrast grating was presented in the top location; no such grating appeared between trials in the control condition. Contrast matches showed a clear reduction during the adaptation condition, thus demonstrating perceptual fading and a successful replication of Blakemore et al. (1971) We then simplified the approach and modified the code to create a single, seamless experience for use in the classroom. With instructions and theoretical background provided in a one-page handout, students can perform the experiment on themselves and view their results in an automatically generated figure. This exercise, a primary example of active learning, will help students gain a first-hand understanding of the perceptual effects of adaptation.
... In addition, we assess the linearity or nonlinearity of the HDRs induced by different stimulation durations in the primary auditory cortex. This analysis aims to improve the design of fNIRS auditory experiments when task duration varies (Soltysik et al., 2004) and to increase the understanding of brain adaptation peculiarities (Krekelberg et al., 2006). Furthermore, although the effects of stimulus duration have been extensively reported in previous studies using fMRI, no standardized stimulation duration has yet been proposed. ...
Functional near-infrared spectroscopy (fNIRS) is an increasingly popular method in hearing research. However, few studies have considered efficient stimulation parameters for fNIRS auditory experimental design. The objectives of our study are (1) to characterize the auditory hemodynamic responses to trains of white noise with increasing stimulation durations (8s, 10s, 15s, 20s) in terms of amplitude and response linearity; (2) to identify the most-efficient stimulation duration using fNIRS; and (3) to generalize results to more ecological environmental stimuli. We found that cortical activity is augmented following the increments in stimulation durations and reaches a plateau after about 15s of stimulation. The linearity analysis showed that this augmentation due to stimulation duration is not linear in the auditory cortex, the non-linearity being more pronounced for longer durations (15s and 20s). The 15s block duration that we propose as optimal precludes signal saturation, is associated with a high response amplitude and a relatively short total experimental duration. Moreover, the 15s duration remains optimal independently of the nature of presented sounds. The sum of these findings suggests that 15s stimulation duration used in the appropriate experimental setup allows researchers to acquire optimal fNIRS signal quality.
... A classic finding across multiple methods of recording neural activity -from BOLD fMRI, to scalp electrophysiology, to recordings from individual neurons -is that repeated presentation of the same stimulus attenuates neural response (Grill-Spector et al., 2006). While the signal differences measured as population-level neural activity via neuroimaging doubtlessly reflect the aggregate change in response over many different mechanisms of short-term plasticity (Krekelberg et al., 2006;Larsson et al., 2016), some of these changes are strictly feedforward, in that they alter neural responses in the absence of top-down behavioral demands or when stimulus repetition is unexpected (e.g., Larsson & Smith, 2012). Instead of a failure to generate the top-down neuromodulatory signals that tune neuronal responses in expectation of particular stimulus features (as discussed above), the neural adaptation deficits previously observed in dyslexia could have been attributable to differences in strictly bottom-up processing that reduce the ability of population-level recordings like EEG and fMRI to detect repetitioninduced changes in neural response. ...
A perceptual adaptation deficit often accompanies reading difficulty in dyslexia, manifesting in poor perceptual learning of consistent stimuli and reduced neurophysiological adaptation to stimulus repetition. However, it is not known how adaptation deficits relate to differences in feedforward or feedback processes in the brain. Here we used electroencephalography (EEG) to interrogate the feedforward and feedback contributions to neural adaptation as adults with and without dyslexia viewed pairs of faces and words in a paradigm that manipulated whether there was a high probability of stimulus repetition versus a high probability of stimulus change. We measured three neural dependent variables: expectation (the difference between prestimulus EEG power with and without the expectation of stimulus repetition), feedforward repetition (the difference between event-related potentials (ERPs) evoked by an expected change and an unexpected repetition), and feedback-mediated prediction error (the difference between ERPs evoked by an unexpected change and an expected repetition). Expectation significantly modulated prestimulus theta- and alpha-band EEG in both groups. Unexpected repetitions of words, but not faces, also led to significant feedforward repetition effects in the ERPs of both groups. However, neural prediction error when an unexpected change occurred instead of an expected repetition was significantly weaker in dyslexia than the control group for both faces and words. These results suggest that the neural and perceptual adaptation deficits observed in dyslexia reflect the failure to effectively integrate perceptual predictions with feedforward sensory processing. In addition to reducing perceptual efficiency, the attenuation of neural prediction error signals would also be deleterious to the wide range of perceptual and procedural learning abilities that are critical for developing accurate and fluent reading skills.
The left ventral occipitotemporal cortex (lvOT) has been consistently identified as a crucial structure in word reading, and its function varies across subregions. Nevertheless, the specific function of the lvOT and its subregions remains controversial because the obvious grapheme‐to‐phoneme correspondence rules of alphabetic languages make it difficult to disentangle the contributions of orthography and phonology to neural activations. To explore information processing in lvOT subregions, the present study manipulated the orthography and phonology in a factorial design and used the fMRI rapid adaptation paradigm. The results revealed a posterior‐to‐anterior functional gradient in lvOT in Chinese word reading and specified that the functional transition from sublexical to lexical processing occurred in the middle subregion close to the classic VWFA. More importantly, we found that the middle and posterior subregions of lvOT are responsible for processing both orthographic and phonological information during Chinese word reading. These results elaborated the function of the lvOT in Chinese word reading.
The human brain possesses neural networks and mechanisms enabling the representation of numbers, basic arithmetic operations, and mathematical reasoning. Without the ability to represent numerical quantity and perform calculations, our scientifically and technically advanced culture would not exist. However, the origins of numerical abilities are grounded in an intuitive understanding of quantity deeply rooted in biology. Nevertheless, more advanced symbolic arithmetic skills necessitate a cultural background with formal mathematical education. In the past two decades, cognitive neuroscience has seen significant progress in understanding the workings of the calculating brain through various methods and model systems. This review begins by exploring the mental and neuronal representations of non-symbolic numerical quantity, then progresses to symbolic representations acquired in childhood. During arithmetic operations (addition, subtraction, multiplication, and division), these representations are processed and transformed according to arithmetic rules and principles, leveraging different mental strategies and types of arithmetic knowledge that can be dissociated in the brain. While it was once believed that number processing and calculation originated from the language faculty, it is now evident that mathematical and linguistic abilities are primarily processed independently in the brain. Understanding how the healthy brain processes numerical information is crucial for gaining insights into debilitating numerical disorders, including acquired conditions like acalculia and learning-related calculation disorders such as developmental dyscalculia.
Neuroscientific research on emotion has developed dramatically over the past decade. The cognitive neuroscience of human emotion, which has emerged as the new and thriving area of 'affective neuroscience', is rapidly rendering existing overviews of the field obsolete. This handbook provides a comprehensive, up-to-date and authoritative survey of knowledge and topics investigated in this cutting-edge field. It covers a range of topics, from face and voice perception to pain and music, as well as social behaviors and decision making. The book considers and interrogates multiple research methods, among them brain imaging and physiology measurements, as well as methods used to evaluate behavior and genetics. Editors Jorge Armony and Patrik Vuilleumier have enlisted well-known and active researchers from more than twenty institutions across three continents, bringing geographic as well as methodological breadth to the collection. This timely volume will become a key reference work for researchers and students in the growing field of neuroscience.
Neuroscientific research on emotion has developed dramatically over the past decade. The cognitive neuroscience of human emotion, which has emerged as the new and thriving area of 'affective neuroscience', is rapidly rendering existing overviews of the field obsolete. This handbook provides a comprehensive, up-to-date and authoritative survey of knowledge and topics investigated in this cutting-edge field. It covers a range of topics, from face and voice perception to pain and music, as well as social behaviors and decision making. The book considers and interrogates multiple research methods, among them brain imaging and physiology measurements, as well as methods used to evaluate behavior and genetics. Editors Jorge Armony and Patrik Vuilleumier have enlisted well-known and active researchers from more than twenty institutions across three continents, bringing geographic as well as methodological breadth to the collection. This timely volume will become a key reference work for researchers and students in the growing field of neuroscience.
Neuroscientific research on emotion has developed dramatically over the past decade. The cognitive neuroscience of human emotion, which has emerged as the new and thriving area of 'affective neuroscience', is rapidly rendering existing overviews of the field obsolete. This handbook provides a comprehensive, up-to-date and authoritative survey of knowledge and topics investigated in this cutting-edge field. It covers a range of topics, from face and voice perception to pain and music, as well as social behaviors and decision making. The book considers and interrogates multiple research methods, among them brain imaging and physiology measurements, as well as methods used to evaluate behavior and genetics. Editors Jorge Armony and Patrik Vuilleumier have enlisted well-known and active researchers from more than twenty institutions across three continents, bringing geographic as well as methodological breadth to the collection. This timely volume will become a key reference work for researchers and students in the growing field of neuroscience.
Groupitizing is a well-established strategy in numerosity perception that enhances speed and sensory precision. Building on the ATOM theory, Anobile proposed the sensorimotor numerosity system, which posits a strong link between number and action. Previous studies using motor adaptation technology have shown that high-frequency motor adaptation leads to underestimation of numerosity perception, while low-frequency adaptation leads to overestimation. However, the impact of motor adaptation on groupitizing, and whether visual motion adaptation produces similar effects, remain unclear. In this study, we investigate the persistence of the advantage of groupitizing after motor adaptation and explore the effects of visual motion adaptation. Surprisingly, our findings reveal that proprioceptive motor adaptation weakens the advantage of groupitizing, indicating a robust effect of motor adaptation even when groupitizing is employed. Moreover, we observe a bidirectional relationship, as groupitizing also weakens the adaptation effect. These results highlight the complex interplay between motor adaptation and groupitizing in numerosity perception. Furthermore, our study provides evidence that visual motion adaptation also has an adaptation effect, but does not fully replicate the effects of proprioceptive motor adaptation on groupitizing. In conclusion, our research underscores the importance of groupitizing as a valuable strategy in numerosity perception, and sheds light on the influence of motion adaptation on this strategy.
Artificial intelligence (AI) is a fast-growing field focused on modeling and machine implementation of various cognitive functions with an increasing number of applications in computer vision, text processing, robotics, neurotechnology, bio-inspired computing and others. In this chapter, we describe how AI methods can be applied in the context of intracranial electroencephalography (iEEG) research. IEEG data is unique as it provides extremely high-quality signals recorded directly from brain tissue. Applying advanced AI models to this data carries the potential to further our understanding of many fundamental questions in neuroscience. At the same time, as an invasive technique, iEEG lends itself well to long-term, mobile brain-computer interface applications, particularly for communication in severely paralyzed individuals. We provide a detailed overview of these two research directions in the application of AI techniques to iEEG. That is, (1) the development of computational models that target fundamental questions about the neurobiological nature of cognition (AI-iEEG for neuroscience) and (2) applied research on monitoring and identification of event-driven brain states for the development of clinical brain-computer interface systems (AI-iEEG for neurotechnology). We explain key machine learning concepts, specifics of processing and modeling iEEG data and details of state-of-the-art iEEG-based neurotechnology and brain-computer interfaces.
One prominent feature of the infraslow BOLD signal during rest or task is quasi-periodic spatiotemporal pattern (QPP) of signal changes that involves an alternation of activity in key functional networks and propagation of activity across brain areas, and that is known to tie to the infraslow neural activity involved in attention and arousal fluctuations. This ongoing whole-brain pattern of activity might potentially modify the response to incoming stimuli or be modified itself by the induced neural activity. To investigate this, we presented checkerboard sequences flashing at 6Hz to subjects. This is a salient visual stimulus that is known to produce a strong response in visual processing regions. Two different visual stimulation sequences were employed, a systematic stimulation sequence in which the visual stimulus appeared every 20.3 secs and a random stimulation sequence in which the visual stimulus occurred randomly every 14~62.3 secs. Three central observations emerged. First, the two different stimulation conditions affect the QPP waveform in different aspects, i.e., systematic stimulation has greater effects on its phase and random stimulation has greater effects on its magnitude. Second, the QPP was more frequent in the systematic condition with significantly shorter intervals between consecutive QPPs compared to the random condition. Third, the BOLD signal response to the visual stimulus across both conditions was swamped by the QPP at the stimulus onset. These results provide novel insights into the relationship between intrinsic patterns and stimulated brain activity.
The existence of a neural representation for whole words (i.e., a lexicon) is a common feature of many models of speech processing. Prior studies have provided evidence for a visual lexicon containing representations of whole written words in an area of the ventral visual stream known as the “Visual Word Form Area” (VWFA). Similar experimental support for an auditory lexicon containing representations of spoken words has yet to be shown. Using fMRI rapid adaptation techniques, we provide evidence for an auditory lexicon in the “Auditory Word Form Area” (AWFA) in the human left anterior superior temporal gyrus that contains representations highly selective for individual spoken words. Furthermore, we show that familiarization with novel auditory words sharpens the selectivity of their representations in the AWFA. These findings reveal strong parallels in how the brain represents written and spoken words, showing convergent processing strategies across modalities in the visual and auditory ventral streams.
Repeated exposure to a stimulus results in reduced neural response, or repetition suppression, in brain regions responsible for processing that stimulus. This rapid accommodation to repetition is thought to underlie learning, stimulus selectivity, and strengthening of perceptual expectations. Importantly, reduced sensitivity to repetition has been identified in several neurodevelopmental, learning, and psychiatric disorders including autism spectrum disorder (ASD) - a neurodevelopmental disorder characterized by challenges in social communication and repetitive behaviors and restricted interests. Reduced ability to exploit or learn from repetition in ASD is hypothesized to contribute to sensory hypersensitivities, and parallels several theoretical frameworks claiming that ASD individuals show difficulty using regularities in the environment to facilitate behavior. Using functional magnetic resonance imaging (fMRI) in autistic and neurotypical human adults (females and males), we assessed the status of repetition suppression across two modalities (vision, audition) and with four stimulus categories (faces, objects, printed words, and spoken words). ASD individuals showed domain-specific reductions in repetition suppression for face stimuli only, but not for objects, printed words, or spoken words. Reduced repetition suppression for faces was associated with greater challenges in social communication in ASD. We also found altered functional connectivity between atypically adapting cortical regions and higher-order face recognition regions and microstructural differences in related white matter tracts in ASD. These results suggest that fundamental neural mechanisms and system-wide circuits are selectively altered for face processing in ASD and enhance our understanding of how disruptions in the formation of stable face representations may relate to higher-order social communication processes.
SIGNIFICANCE STATEMENT
A common finding in neuroscience is that repetition results in plasticity in stimulus-specific processing regions, reflecting selectivity and adaptation (repetition suppression, RS). RS is reduced in several neurodevelopmental and psychiatric disorders, including autism spectrum disorder (ASD). Theoretical frameworks of ASD posit that reduced adaptation may contribute to associated challenges in social communication and sensory processing. However, the scope of RS differences in ASD are unknown. We examined RS for multiple categories across visual and auditory domains (faces, objects, printed words, spoken words) in autistic and neurotypical individuals. We found reduced RS in ASD for face stimuli only and altered functional connectivity and white matter microstructure between cortical face-recognition areas. RS magnitude correlated with social communication challenges among autistic individuals.
Faces are thought to have a privileged status for processing relative to other visual images. Humans use faces to identify people, learn language, and to communicate and understand intentions, meaning and emotions. An enduring debate within the fields of developmental psychology and cognitive neuroscience is whether human face processing is specialized owing to domain-specific neural circuitry driven primarily by evolutionary mechanisms or whether it emerges from a domain-general architecture through experience. In this Perspective, we argue for an experience-based account based on associative and non-associative learning and supported by general neurobiological mechanisms. We posit that face-processing specialization emerges from activity-dependent, self-organizing processes where neuronal connectivity is shaped by the environment and constrained by intrinsic yet malleable neural architecture. This ‘domain-relevant’ framework for face processing reflects a dynamic interaction between the developing brain and the environmental input. Whether human face-processing specialization arrives innately at birth or arises through experience across development is an enduring debate. In this Perspective, Scott and Arcaro argue for an experience-based account whereby face-processing specialization emerges from associative and non-associative learning constrained by intrinsic neurobiological mechanisms.
Probability distortion—the tendency to underweight larger probabilities and overweight smaller ones—is a robust empirical phenomenon and an important driver of suboptimal choices. We reveal a novel contextual effect on probability distortion that depends on the composition of the choice set. Probability distortion was larger in a magnitude-diverse choice set (in which participants encountered more unique magnitudes than probabilities) but declined, resulting in more veridical weighting, in a probability-diverse choice set (more unique probabilities than magnitudes). This effect was consistent in two, large, independent datasets (N = 481, N = 100) and held for a subset of lotteries that were identical in the two contexts. It also developed gradually as a function of exposure to the choice set, was independent of attentional biases to probability versus magnitude information, and was specific to probability weighting, leaving risk attitudes unaffected. The results highlight the importance of context when processing probabilistic information.
Our experience of time can feel dilated or compressed, rather than reflecting true “clock time.” Although many contextual factors influence the subjective perception of time, it is unclear how memory accessibility plays a role in constructing our experience of and memory for time. Here, we used a combination of behavioral and functional MRI measures in healthy young adults ( N = 147) to ask the question of how memory is incorporated into temporal duration judgments. Behaviorally, we found that event boundaries, which have been shown to disrupt ongoing memory integration processes, result in the temporal compression of duration judgments. Additionally, using a multivoxel pattern similarity analysis of functional MRI data, we found that greater temporal pattern change in the left hippocampus within individual trials was associated with longer duration judgments. Together, these data suggest that mnemonic processes play a role in constructing representations of time.
Processing more likely inputs with higher sensitivity (adaptive coding) enables the brain to represent the large range of inputs coming in from the world. Healthy individuals high in schizotypy show reduced adaptive coding in the reward domain but it is an open question whether these deficits extend to non-motivational domains, such as object categorization. Here, we develop a novel variant of a classic task to test range adaptation for face/house categorization in healthy participants on the psychosis spectrum. In each trial of this task, participants decide whether a presented image is a face or a house. Images vary on a face-house continuum and appear in both wide and narrow range blocks. The wide range block includes most of the face-house continuum (2.50–97.5% face), while the narrow range blocks limit inputs to a smaller section of the continuum (27.5–72.5% face). Adaptive coding corresponds to better performance for the overlapping smaller section of the continuum in the narrow range than in the wide range block. We find that participants show efficient use of the range in this task, with more accurate responses in the overlapping section for the narrow range blocks relative to the wide range blocks. However, we find little evidence that range adaptation in our object categorization task is reduced in healthy individuals scoring high on schizotypy. Thus, reduced range adaptation may not be a domain-general feature of schizotypy.
The idea that visual coding and perception are shaped by experience and adjust to changes in the environment or the observer is universally recognized as a cornerstone of visual processing, yet the functions and processes mediating these calibrations remain in many ways poorly understood. In this article we review a number of facets and issues surrounding the general notion of calibration, with a focus on plasticity within the encoding and representational stages of visual processing. These include how many types of calibrations there are – and how we decide; how plasticity for encoding is intertwined with other principles of sensory coding; how it is instantiated at the level of the dynamic networks mediating vision; how it varies with development or between individuals; and the factors that may limit the form or degree of the adjustments. Our goal is to give a small glimpse of an enormous and fundamental dimension of vision, and to point to some of the unresolved questions in our understanding of how and why ongoing calibrations are a pervasive and essential element of vision.
The existence of a neural representation for whole words (i.e., a lexicon) is a common feature of many models of speech processing. Prior studies have provided evidence for a visual lexicon containing representations of whole written words in an area of the ventral visual stream known as the “Visual Word Form Area” (VWFA). Similar experimental support for an auditory lexicon containing representations of spoken words has yet to be shown. Using fMRI rapid adaptation techniques, we provide evidence for an auditory lexicon in the “Auditory Word Form Area” (AWFA) in the human left anterior superior temporal gyrus that contains representations highly selective for individual spoken words. Furthermore, we show that familiarization with novel auditory words sharpens the selectivity of their representations in the AWFA. These findings reveal strong parallels in how the brain represents written and spoken words, showing convergent processing strategies across modalities in the visual and auditory ventral streams.
Highlights
Individual auditory word form areas (AWFA) were defined via an auditory localizer
The AWFA shows tuning for individual real words but not untrained pseudowords
The AWFA develops tuning for individual pseudowords after training
Contrast adaptation is a fundamental visual process that has been extensively investigated and used to infer the selectivity of visual cortex. We recently reported an apparent disconnect between the effects of contrast adaptation on perception and functional magnetic resonance imaging BOLD response adaptation, in which adaptation between chromatic and achromatic stimuli measured psychophysically showed greater selectivity than adaptation measured using BOLD signals. Here we used magnetoencephalography (MEG) recordings of neural responses to the same chromatic and achromatic adaptation conditions to characterize the neural effects of contrast adaptation and to determine whether BOLD adaptation or MEG better reflect the measured perceptual effects. Participants viewed achromatic, L-M isolating, or S-cone isolating radial sinusoids before adaptation and after adaptation to each of the three contrast directions. We measured adaptation-related changes in the neural response to a range of stimulus contrast amplitudes using two measures of the MEG response: the overall response amplitude, and a novel time-resolved measure of the contrast response function, derived from a classification analysis combined with multidimensional scaling. Within-stimulus adaptation effects on the contrast response functions in each case showed a pattern of contrast-gain or a combination of contrast-gain and response-gain effects. Cross-stimulus adaptation conditions showed that adaptation effects were highly stimulus selective across early, ventral, and dorsal visual cortical areas, consistent with the perceptual effects.
Functional near-infrared spectroscopy (fNIRS) is an increasingly popular method in hearing research. However, few studies have considered efficient stimulation parameters for the auditory experimental design of fNIRS. The objectives of our study are (1) to identify the most effective paradigm for the stimulation blocks with increasing duration (8s, 10s, 15s, 20s) in terms of response amplitude, i.e., the most-efficient stimulation duration; (2) to assess the linearity/nonlinearity of the hemodynamic responses with respect to increasing block durations; and (3) to generalize results to more ecological environmental stimuli. We found that cortical activity is augmented following the increments in stimulation durations and reaches a plateau after about 15s of stimulation. The linearity analysis showed that this augmentation due to stimulation duration is not linear in the auditory cortex, non-linearity being more pronounced for longer durations (15s and 20s). The 15s block duration that we propose as the most suitable precludes signal saturation and is associated with a high response amplitude and a relatively short total experimental duration. Moreover, the distribution of stimuli among the 15s blocks remains the most effective for white noise stimulation and also provides a comparably strong response for environmental sounds. The sum of these findings suggests that 15s stimulation duration used in the appropriate experimental setup allows researchers to acquire optimal fNIRS signal quality.
Identifying the faces of familiar persons requires the ability to assign several different images of a face to a common identity. Previous research showed that the occipito‐temporal cortex, including the fusiform and the occipital face areas, is sensitive to personal identity. Still, the viewpoint, facial expression, and image‐independence of this information are currently under heavy debate. Here we adapted a rapid serial visual stimulation paradigm (Johnston et al., 2016) and presented highly variable ambient‐face images of famous persons to measure fMRI adaptation. FMRI adaptation is considered as the neuroimaging manifestation of repetition suppression, a neural phenomenon currently explained as a correlate of reduced predictive error responses for expected stimuli. We revisited the question of image‐invariant identity‐specific encoding mechanisms of the occipito‐temporal cortex, using fMRI adaptation with a particular interest in predictive mechanisms. Participants were presented with trials containing eight different images of a famous person, images of eight different famous persons, or seven different images of a particular famous person followed by an identity change to violate potential expectation effects about person identity. We found an image‐independent adaptation effect of identity for famous faces in the fusiform face area. However, in contrast to previous electrophysiological studies, using similar paradigms, no release of the adaptation effect was observed when identity‐specific expectations were violated. Our results support recent multivariate pattern analysis studies, showing image‐independent identity encoding in the core face‐processing areas of the occipito‐temporal cortex. These results are discussed in the frame of recent identity‐processing models and predictive mechanisms.
A perceptual adaptation deficit often accompanies reading difficulty in dyslexia, manifesting in poor perceptual learning of consistent stimuli and reduced neurophysiological adaptation to stimulus repetition. However, it is not known how adaptation deficits relate to differences in feedforward or feedback processes in the brain. Here we used electroencephalography (EEG) to interrogate the feedforward and feedback contributions to neural adaptation as adults with and without dyslexia viewed pairs of faces and words in a paradigm that manipulated whether there was a high probability of stimulus repetition versus a high probability of stimulus change. We measured three neural dependent variables: expectation (the difference between prestimulus EEG power with and without the expectation of stimulus repetition), feedforward repetition (the difference between event-related potentials (ERPs) evoked by an expected change and an unexpected repetition), and feedback-mediated prediction error (the difference between ERPs evoked by an unexpected change and an expected repetition). Expectation significantly modulated prestimulus theta- and alpha-band EEG in both groups. Unexpected repetitions of words, but not faces, also led to significant feedforward repetition effects in the ERPs of both groups. However, neural prediction error when an unexpected change occurred instead of an expected repetition was significantly weaker in dyslexia than the control group for both faces and words. These results suggest that the neural and perceptual adaptation deficits observed in dyslexia reflect the failure to effectively integrate perceptual predictions with feedforward sensory processing. In addition to reducing perceptual efficiency, the attenuation of neural prediction error signals would also be deleterious to the wide range of perceptual and procedural learning abilities that are critical for developing accurate and fluent reading skills.
Fast fMRI enables the detection of neural dynamics over timescales of hundreds of milliseconds, suggesting it may provide a new avenue for studying subsecond neural processes in the human brain. The magnitudes of these fast fMRI dynamics are far greater than predicted by canonical models of the hemodynamic response. Several studies have established nonlinear properties of the hemodynamic response that have significant implications for fast fMRI. We first review nonlinear properties of the hemodynamic response function that may underlie fast fMRI signals. We then illustrate the breakdown of canonical hemodynamic response models in the context of fast neural dynamics. We will then argue that the canonical hemodynamic response function is not likely to reflect the BOLD response to neuronal activity driven by sparse or naturalistic stimuli or perhaps to spontaneous neuronal fluctuations in the resting state. These properties suggest that fast fMRI is capable of tracking surprisingly fast neuronal dynamics, and we discuss the neuroscientific questions that could be addressed using this approach.
Cells selectively responsive to the face have been found in several visual sub-areas of temporal cortex in the macaque brain. These include the lateral and ventral surfaces of inferior temporal cortex and the upper bank, lower bank and fundus of the superior temporal sulcus (STS). Cells in the different regions may contribute in different ways to the processing of the facial image. Within the upper bank of the STS different populations of cells are selective for different views of the face and head. These cells occur in functionally discrete patches (3-5 mm across) within the STS cortex. Studies of output connections from the STS also reveal a modular anatomical organization of repeating 3-5 mm patches connected to the parietal cortex, an area thought to be involved in spatial awareness and in the control of attention. The properties of some cells suggest a role in the discrimination of heads from other objects, and in the recognition of familiar individuals. The selectivity for view suggests that the neural operations underlying face or head recognition rely on parallel analyses of different characteristic views of the head, the outputs of these view-specific analyses being subsequently combined to support view-independent (object-centred) recognition. An alternative functional interpretation of the sensitivity to head view is that the cells enable an analysis of 'social attention', i.e. they signal where other individuals are directing their attention. A cell maximally responsive to the left profile thus provides a signal that the attention (of another individual) is directed to the observer's left. Such information is useful for analysing social interactions between other individuals.(ABSTRACT TRUNCATED AT 250 WORDS)
Functional magnetic resonance imaging (fMRI) was used to measure local haemodynamic changes (reflecting electrical activity) in human visual cortex during production of the visual motion aftereffect, also known as the waterfall illusion. As in previous studies, human cortical area MT (V5) responded much better to moving than to stationary visual stimuli. Here we demonstrate a clear increase in activity in MT when subjects viewed a stationary stimulus undergoing illusory motion, following adaptation to stimuli moving in a single local direction. Control stimuli moving in reversing, opposed directions produced neither a perceptual motion aftereffect nor elevated fMRI levels postadaptation. The time course of the motion aftereffect (measured in parallel psychophysical tests) was essentially identical to the time course of the fMRI motion aftereffect. Because the motion aftereffect is direction specific, this indicates that cells in human area MT are also direction specific. In five other retinotopically defined cortical areas, similar motion-specific aftereffects were smaller than those in MT or absent.
The linear transform model of functional magnetic resonance imaging (fMRI) hypothesizes that fMRI responses are proportional to local average neural activity averaged over a period of time. This work reports results from three empirical tests that support this hypothesis. First, fMRI responses in human primary visual cortex (V1) depend separably on stimulus timing and stimulus contrast. Second, responses to long-duration stimuli can be predicted from responses to shorter duration stimuli. Third, the noise in the fMRI data is independent of stimulus contrast and temporal period. Although these tests can not prove the correctness of the linear transform model, they might have been used to reject the model. Because the linear transform model is consistent with our data, we proceeded to estimate the temporal fMRI impulse-response function and the underlying (presumably neural) contrast-response function of human V1.
Human area V1 offers an excellent opportunity to study, using functional MRI, a range of properties in a specific cortical visual area, whose borders are defined objectively and convergently by retinotopic criteria. The retinotopy in V1 (also known as primary visual cortex, striate cortex, or Brodmann's area 17) was defined in each subject by using both stationary and phase-encoded polar coordinate stimuli. Data from V1 and neighboring retinotopic areas were displayed on flattened cortical maps. In additional tests we revealed the paired cortical representations of the monocular "blind spot." We also activated area V1 preferentially (relative to other extrastriate areas) by presenting radial gratings alternating between 6% and 100% contrast. Finally, we showed evidence for orientation selectivity in V1 by measuring transient functional MRI increases produced at the change in response to gratings of differing orientations. By systematically varying the orientations presented, we were able to measure the bandwidth of the orientation "transients" (45 degrees).
Electrophysiological studies indicate that neurons in the middle temporal (MT) area of the primate brain are selective for the velocity of visual stimuli. This paper describes a computational model of MT physiology, in which local image velocities are represented via the distribution of MT neuronal responses. The computation is performed in two stages, corresponding to neurons in cortical areas V1 and MT. Each stage computes a weighted linear sum of inputs, followed by rectification and divisive normalization. V1 receptive field weights are designed for orientation and direction selectivity. MT receptive field weights are designed for velocity (both speed and direction) selectivity. The paper includes computational simulations accounting for a wide range of physiological data, and describes experiments that could be used to further test and refine the model.
The responsiveness of neurons in the primary visual cortex (V1) is substantially reduced after a few seconds of visual stimulation with an effective pattern. This phenomenon, called pattern adaptation, is uniquely cortical and is the likely substrate of a variety of perceptual after-effects. While adaptation to a given pattern reduces the responses of V1 neurons to all subsequently viewed test patterns, this reduction shows some specificity, being strongest when the adapting and test patterns are identical. This specificity may indicate that adaptation affects the interaction between groups of neurons that are jointly activated by the adapting stimulus. We investigated this possibility by studying the effects of adaptation to visual patterns containing one or both of two orientations--the preferred orientation for a cell, and the orientation orthogonal to it. Because neurons in the primary visual cortex are sharply tuned for orientation, stimulation with orthogonal orientations excites two largely distinct populations of neurons. With intracellular recordings of the membrane potential of cat V1 neurons, we found that adaptation to the orthogonal orientation alone does not evoke the hyperpolarization that is typical of adaptation to the preferred orientation. With extracellular recordings of the firing rate of macaque V1 neurons, we found that the responses were not reduced by adaptation to the orthogonal orientation alone nearly as much as by adaptation to the preferred orientation. In the macaque we also studied the effects of adaptation to plaids containing both the preferred and the orthogonal orientations. We found that adaptation to these stimuli could modify the interactions between orientations. It increased the amount of cross-orientation suppression displayed by some cells, even turning some cells that showed cross-orientation facilitation when adapted to a blank stimulus into cells that show cross-orientation suppression. This result suggests that pattern adaptation can affect the interaction between the groups of neurons tuned to the orthogonal orientations, either by increasing their mutual inhibition or by decreasing their mutual excitation.
Complex cells in striate cortex of macaque showed a rapid pattern-specific adaptation. Adaptation made cells more sensitive
to orientation change near the adapting orientation. It reduced correlations among the responses of populations of cells,
thereby increasing the information transmitted by each action potential. These changes were brought about by brief exposures
to stationary patterns, on the time scale of a single fixation. Thus, if successive fixations expose neurons' receptive fields
to images with similar but not identical structure, adaptation will remove correlations and improve discriminability.
Face perception, perhaps the most highly developed visual skill in humans, is mediated by a distributed neural system in humans that is comprised of multiple, bilateral regions. We propose a model for the organization of this system that emphasizes a distinction between the representation of invariant and changeable aspects of faces. The representation of invariant aspects of faces underlies the recognition of individuals, whereas the representation of changeable aspects of faces, such as eye gaze, expression, and lip movement, underlies the perception of information that facilitates social communication. The model is also hierarchical insofar as it is divided into a core system and an extended system. The core system is comprised of occipitotemporal regions in extrastriate visual cortex that mediate the visual analysis of faces. In the core system, the representation of invariant aspects is mediated more by the face-responsive region in the fusiform gyrus, whereas the representation of changeable aspects is mediated more by the face-responsive region in the superior temporal sulcus. The extended system is comprised of regions from neural systems for other cognitive functions that can be recruited to act in concert with the regions in the core system to extract meaning from faces.
The origin of orientation selectivity in the responses of simple cells in cat visual cortex serves as a model problem for understanding cortical circuitry and computation. The feed-forward model posits that this selectivity arises simply from the arrangement of thalamic inputs to a simple cell. Much evidence, including a number of recent intracellular studies, supports a primary role of the thalamic inputs in determining simple cell response properties, including orientation tuning. This mechanism alone, however, cannot explain the invariance of orientation tuning to changes in stimulus contrast. Simple cells receive push-pull inhibition: ON inhibition in OFF subregions and vice versa. Addition of such inhibition to the feed-forward model can account for this contrast invariance, provided the inhibition is sufficiently strong. The predictions of "normalization" and "feedback" models are reviewed and compared with the predictions of this modified feed-forward model and with experimental results. The modified feed-forward and the feedback models ascribe fundamentally different functions to cortical processing.
We used high-level configural aftereffects induced by adaptation to realistic faces to investigate visual representations underlying complex pattern perception. We found that exposure to an individual face for a few seconds generated a significant and precise bias in the subsequent perception of face identity. In the context of a computationally derived 'face space,' adaptation specifically shifted perception along a trajectory passing through the adapting and average faces, selectively facilitating recognition of a test face lying on this trajectory and impairing recognition of other faces. The results suggest that the encoding of faces and other complex patterns draws upon contrastive neural mechanisms that reference the central tendency of the stimulus category.
The functional architecture of the object vision pathway in the human brain was investigated using functional magnetic resonance
imaging to measure patterns of response in ventral temporal cortex while subjects viewed faces, cats, five categories of man-made
objects, and nonsense pictures. A distinct pattern of response was found for each stimulus category. The distinctiveness of
the response to a given category was not due simply to the regions that responded maximally to that category, because the
category being viewed also could be identified on the basis of the pattern of response when those regions were excluded from
the analysis. Patterns of response that discriminated among all categories were found even within cortical regions that responded
maximally to only one category. These results indicate that the representations of faces and objects in ventral temporal cortex
are widely distributed and overlapping.
Several fMRI studies have reported MT+ response increases correlated with perception of the motion aftereffect (MAE). However, attention can strongly affect MT+ responses, and subjects may naturally attend more to the MAE than control trials without MAE. We found that requiring subjects to attend to motion on both MAE and control trials produced equal levels of MT+ response, suggesting that attention may have confounded the interpretation of previous experiments; in our data, attention accounts for the entire effect. After eliminating this confound, we observed that direction-selective motion adaptation produced a direction-selective imbalance in MT+ responses (and earlier visual areas), and yielded a corresponding asymmetry in speed discrimination thresholds. These findings provide physiological evidence that population level response imbalances underlie the MAE, and quantify the relative proportions of direction-selective neurons across human visual areas.
A striking aspect of natural scenes is that image features such as line orientation are strongly correlated at neighboring spatial locations but not at distant locations. Thus, during the viewing of a scene, eye movements are often accompanied by a change in the orientation structure of the image. How does this behavior influence the discrimination of local features and their encoding by visual cortical neurons? Here we examined the perceived changes in orientation induced by brief exposure to oriented image patterns in monkeys and humans, and then used reverse correlation to investigate dynamic changes in neuronal sensitivity in the primary visual cortex (V1) of behaving monkeys. Whereas brief adaptation to an oriented grating impaired identification of nearby orientations by broadening orientation selectivity and changing the preferred orientation of individual V1 neurons, it actually enhanced the identification of orthogonal orientations by sharpening neuronal selectivity. Hence, successive exposure to image patches of dissimilar spatial structure enhances both the ability to discriminate local features and the encoding of these features by V1 neurons.
Motion of an object is thought to be perceived independently of the object's surface properties. However, theoretical, neuropsychological and psychophysical observations have suggested that motion of textures, called 'second-order motion', may be processed by a separate system from luminance-based, or 'first-order', motion. Functional magnetic resonance imaging (fMRI) responses during passive viewing, attentional modulation and post-adaptation motion after-effects (MAE) of these stimuli were measured in seven retinotopic visual areas (labeled V1, V2, V3, VP, V4v, V3A and LO) and the motion-sensitive area MT/MST (V5). In all visual areas, responses were strikingly similar to motion of first- and second-order stimuli. These results differ from a prior investigation, because here the motion-specific responses were isolated. Directing attention towards and away from the motion elicited equivalent response modulation for the two types. Dramatic post-adaptation (MAE) differences in perception of the two stimuli were observed and fMRI activation mimicked perceptual changes, but did not reveal the processing differences. In fact, no visual area was found to respond selectively to the motion of second-order stimuli, suggesting that motion perception arises from a unified motion detection system.
It has been only a decade since functional magnetic resonance imaging (fMRI) was introduced, but approximately four fMRI papers are now published every working day. Here we review this progress in a well studied system: primate visual cortex.
How are different object categories organized by the visual system? Current evidence indicates that monkeys and humans process object categories in fundamentally different ways. Functional magnetic resonance imaging (fMRI) studies suggest that humans have a ventral temporal face area, but such evidence is lacking in macaques. Instead, face-responsive neurons in macaques seem to be scattered throughout temporal cortex, with some relative concentration in the superior temporal sulcus (STS). Here, using fMRI in alert fixating macaque monkeys and humans, we found that macaques do have discrete face-selective patches, similar in relative size and number to face patches in humans. The face patches were embedded within a large swath of object-selective cortex extending from V4 to rostral TE. This large region responded better to pictures of intact objects compared to scrambled objects, with different object categories eliciting different patterns of activity, as in the human. Overall, our results suggest that humans and macaques share a similar brain architecture for visual object processing.
Nearly all methods for analyzing and interpreting functional magnetic resonance imaging (fMRI) data assume that the fMRI signal behaves in an approximately linear manner. However, it has been shown that the mean fMRI response to a pair of briefly presented visual stimuli is significantly smaller than would be expected from the response to a single stimulus. This smaller response could be the result of either a nonlinearity in the fMRI signal or neuronal adaptation. We tested the neuronal adaptation hypothesis by measuring the fMRI response to sequential pairs of sinusoidal gratings that had either the same or orthogonal orientation. The adaptation hypothesis predicts that brain areas with orientation-selective neurons should show a more linear response when the stimulus pair is orthogonal than when the pair is identical. Our results show no orientation-specific adaptation effects in primary visual cortex (V1) but increasing effects along the hierarchy of visual areas (V2, V3, and V4V). A psychophysical contrast detection experiment, using similar oriented gratings as adapters, shows evidence of orientation-specific adaptation in the visual system. These results have implications for the interpretation of rapid event-related fMRI experiments, as well as for recently developed methods that use adaptation as a tool to measure the response properties of underlying neuronal subpopulations.
We show that under natural viewing, the responses of cells the temporal lobe of the macaque to the sight of static head body postures is controlled by the sight of immediately actions. Cells in the anterior part of the superior sulcus responded vigorously to the sight of a face or posture that followed a particular body action, but not when it followed other actions. The effective action or posture presented in isolation or in different sequences failed to produce a response. Our results demonstrate that cells in the temporal cortex could support the formation of expectations about impending behavior of others.
The development of functional magnetic resonance imaging (fMRI) has brought together a broad community of scientists interested in measuring the neural basis of the human mind. Because fMRI signals are an indirect measure of neural activity, interpreting these signals to make deductions about the nervous system requires some understanding of the signaling mechanisms. We describe our current understanding of the causal relationships between neural activity and the blood-oxygen-level-dependent (BOLD) signal, and we review how these analyses have challenged some basic assumptions that have guided neuroscience. We conclude with a discussion of how to use the BOLD signal to make inferences about the neural signal.
Motion of an object is thought to be perceived independently of the object’s surface properties. However, theoretical, neuropsychological and psychophysical observations have suggested that motion of textures, called ‘second-order motion’, may be processed by a separate system from luminance-based, or ‘first-order’, motion. Functional magnetic resonance imaging (fMRI) responses during passive viewing, attentional modulation and post-adaptation motion after-effects (MAE) of these stimuli were measured in seven retinotopic visual areas (labeled V1, V2, V3, VP, V4v, V3A and LO) and the motion-sensitive area MT/MST (V5). In all visual areas, responses were strikingly similar to motion of first- and secondorder stimuli. These results differ from a prior investigation, because here the motion-specific responses were isolated. Directing attention towards and away from the motion elicited equivalent response modulation for the two types. Dramatic post-adaptation (MAE) differences in perception of the two stimuli were observed and fMRI activation mimicked perceptual changes, but did not reveal the processing differences. In fact, no visual area was found to respond selectively to the motion of second-order stimuli, suggesting that motion perception arises from a unified motion detection system.
The integration of local image features into global shapes was investigated in monkeys and humans using fMRI. An adaptation paradigm was used, in which stimulus selectivity was deduced by changes in the course of adaptation of a pattern of randomly oriented elements. Accordingly, we observed stronger activity when orientation changes in the adapting stimulus resulted in a collinear contour than a different random pattern. This selectivity to collinear contours was observed not only in higher visual areas that are implicated in shape processing, but also in early visual areas where selectivity depended on the receptive field size. These findings suggest that unified shape perception in both monkeys and humans involves multiple visual areas that may integrate local elements to global shapes at different spatial scales.
A refined and quantitative investigation of an earlier study which demonstrated that a line seen as tilted somewhat from the vertical or horizontal axis appears less tilted during the course of perception. Evidence from the present experiments reveals that the degree of adaptation toward the vertical and horizontal increases with longer and longer periods of inspection in a time curve similar to those of other processes of adaptation. The tilt-adaptation is never complete, however, but levels off before the quality of tilt is completely eliminated. In another phase of the present investigation it was shown that a negative after-effect on one reference-axis is accompanied by a corresponding indirect effect on the other axis, less in amount than the direct effect. The question as to whether simultaneous contrast between neighboring regions of the visual field can be shown to operate in the perception of tilt is postponed for subsequent treatment. (PsycINFO Database Record (c) 2012 APA, all rights reserved)
We studied the temporal dynamics of motion direction sensitivity in macaque area MT using a motion reverse correlation paradigm. Stimuli consisted of a random sequence of motion steps in eight different directions. Cross-correlating the stimulus with the resulting neural activity reveals the temporal dynamics of direction selectivity. The temporal dynamics of direction selectivity at the preferred speed showed two phases along the time axis: one phase corresponding to an increase in probability for the preferred direction at short latencies and a second phase corresponding to a decrease in probability for the preferred direction at longer latencies. The strength of this biphasic behavior varied between neurons from weak to very strong and was uniformly distributed. Strong biphasic behavior suggests optimal responses for motion steps in the antipreferred direction followed by a motion step in the preferred direction. Correlating spikes to combinations of motion directions corroborates this distinction. The optimal combination for weakly biphasic cells consists of successive steps in the preferred direction, whereas for strongly biphasic cells, it is a reversal of directions. Comparing reverse correlograms to combinations of stimuli to predictions based on correlograms for individual directions revealed several nonlinear effects. Correlations for successive presentations of preferred directions were smaller than predicted, which could be explained by a static nonlinearity (saturation). Correlations to pairs of (nearly) opposite directions were larger than predicted. These results show that MT neurons are generally more responsive when sudden changes in motion directions occur, irrespective of the preferred direction of the neurons. The latter nonlinearities cannot be explained by a simple static nonlinearity at the output of the neuron, but most likely reflect network interactions.
A major limitation in conducting functional neuroimaging studies, particularly for cognitive experiments, has been the use of blocked task paradigms. Here we explored whether selective averaging techniques similar to those applied in event-related potential (ERP) experiments could be used to demonstrate functional magnetic resonance imaging (fMRI) responses to rapidly intermixed trials. In the first two experiments, we observed that for 1-sec trials of full-field visual checkerboard stimulation, the fMRI blood oxygenation level-dependent (BOLD) signal summated in a roughly linear fashion across successive trials even at very short (2 sec and 5 sec) intertrial intervals, although subtle departures from linearity were observed. In experiments 3 and 4, we observed that it is possible to obtain robust activation maps for rapidly presented randomly mixed trial types (left- and right-hemifield visual checkerboard stimulation) spaced as little as 2 sec apart. Taken collectively, these results suggest that selective averaging may enable fMRI experimental designs identical to those used in typical behavioral and ERP studies. The ability to analyze closely spaced single-trial, or event-related, signals provides for a class of experiments which cannot be conducted using blocked designs. Trial types can be randomly intermixed, and selective averaging based upon trial type and/or subject performance is possible.
Single neurons were recorded in owl monkey middle temporal visual cortex (MT). Directional neurons showed direction-selective adaptation to pattern motion: responses to motion in the preferred direction were reduced by adaptation to motion in the preferred direction and enhanced by adaptation in the opposite direction. Non-directional neurons did not show significant adaptation.
1. It was found that an occipital evoked potential can be elicited in the human by moving a grating pattern without changing the mean light flux entering the eye. Prolonged viewing of a high contrast grating reduces the amplitude of the potential evoked by a low contrast grating.
2. This adaptation to a grating was studied psychophysically by determining the contrast threshold before and after adaptation. There is a temporary fivefold rise in contrast threshold after exposure to a high contrast grating of the same orientation and spatial frequency.
3. By determining the rise of threshold over a range of spatial frequency for a number of adapting frequencies it was found that the threshold elevation is limited to a spectrum of frequencies with a bandwidth of just over an octave at half amplitude, centred on the adapting frequency.
4. The amplitude of the effect and its bandwidth are very similar for adapting spatial frequencies between 3 c/deg. and 14 c/deg. At higher frequencies the bandwidth is slightly narrower. For lower adapting frequencies the peak of the effect stays at 3 c/deg.
5. These and other findings suggest that the human visual system may possess neurones selectively sensitive to spatial frequency and size. The orientational selectivity and the interocular transfer of the adaptation effect implicate the visual cortex as the site of these neurones.
6. This neural system may play an essential preliminary role in the recognition of complex images and generalization for magnification.
Using functional magnetic resonance imaging (fMRI), we found an area in the fusiform gyrus in 12 of the 15 subjects tested that was significantly more active when the subjects viewed faces than when they viewed assorted common objects. This face activation was used to define a specific region of interest individually for each subject, within which several new tests of face specificity were run. In each of five subjects tested, the predefined candidate "face area" also responded significantly more strongly to passive viewing of (1) intact than scrambled two-tone faces, (2) full front-view face photos than front-view photos of houses, and (in a different set of five subjects) (3) three-quarter-view face photos (with hair concealed) than photos of human hands; it also responded more strongly during (4) a consecutive matching task performed on three-quarter-view faces versus hands. Our technique of running multiple tests applied to the same region defined functionally within individual subjects provides a solution to two common problems in functional imaging: (1) the requirement to correct for multiple statistical comparisons and (2) the inevitable ambiguity in the interpretation of any study in which only two or three conditions are compared. Our data allow us to reject alternative accounts of the function of the fusiform face area (area "FF") that appeal to visual attention, subordinate-level classification, or general processing of any animate or human forms, demonstrating that this region is selectively involved in the perception of faces.
Studies in primate physiology and human functional neuroimaging have convincingly shown that the area of the brain termed MT/V5(+)-which includes the middle temporal visual area MT/V5 along with adjacent motion-sensitive areas such as MST--is involved in the processing of motion information [1,2]. Tootell et al. [3] showed that the blood oxygenation level dependent (BOLD) signal measured by functional magnetic resonance imaging (fMRI) in the human MT/V5+ seemingly correlates with the strength of perceived motion aftereffect (MAE), the illusory motion of a stationary pattern that one sees after adapting to a moving pattern [4]. The signal in MT/V5+ decayed slowly during the period when the MAE was seen. It is possible that this slow decrease in MT/V5+ activity was unrelated to the perceptual experience of motion. After replicating Tootell et al.'s experiment, a modified version of the experiment was conducted in which a blank period was inserted between the adapting motion stimulus and the stationary testing pattern. The results demonstrated that MT/V5+ activity indeed decayed more slowly after an effective unidirectional motion adaptation than after bidirectional adaptation, without corresponding perception of MAE. Nevertheless, in a more conclusive experiment, we adapted observers to a unidirectional motion for a very long period and showed that the activity in MT/V5+ changed in synchrony with the presence and absence of perceived MAE, simply as a result of presenting a stationary visual stimulus in and out of the adapted retinal region.
When we see a person's face, we can easily recognize their species, individual identity and emotional state. How does the brain represent such complex information? A substantial number of neurons in the macaque temporal cortex respond to faces. However, the neuronal mechanisms underlying the processing of complex information are not yet clear. Here we recorded the activity of single neurons in the temporal cortex of macaque monkeys while presenting visual stimuli consisting of geometric shapes, and monkey and human faces with various expressions. Information theory was used to investigate how well the neuronal responses could categorize the stimuli. We found that single neurons conveyed two different scales of facial information in their firing patterns, starting at different latencies. Global information, categorizing stimuli as monkey faces, human faces or shapes, was conveyed in the earliest part of the responses. Fine information about identity or expression was conveyed later, beginning on average 51 ms after global information. We speculate that global information could be used as a 'header' to prepare destination areas for receiving more detailed information.
A network of brain areas is expected to be involved in supporting the motion aftereffect. The most active components of this network were determined by means of an fMRI study of nine subjects exposed to a visual stimulus of moving bars producing the effect. Across the subjects, common areas were identified during various stages of the effect, as well as networks of areas specific to a single stage. In addition to the well-known motion-sensitive area MT the prefrontal brain areas BA44 and 47 and the cingulate gyrus, as well as posterior sites such as BA37 and BA40, were important components during the period of the motion aftereffect experience. They appear to be involved in control circuitry for selecting which of a number of processing styles is appropriate. The experimental fMRI results of the activation levels and their time courses for the various areas are explored. Correlation analysis shows that there are effectively two separate and weakly coupled networks involved in the total process. Implications of the results for awareness of the effect itself are briefly considered in the final discussion.
We investigated the effects of paired presentations of visual stimuli upon the evoked hemodynamic response of visual cortex measured by magnetic resonance imaging (MRI). Stimuli were identical 500-ms high-contrast checkerboard patterns, presented singly or with an interpair interval (IPI) of 1, 2, 4, or 6 s (onset-to-onset), followed by an intertrial interval of 16-20 s. Images were acquired at 1.5 Tesla using a gradient-echo echoplanar imaging sequence sensitive to blood-oxygenation-level dependent (BOLD) contrast. Single checkerboards evoked a hemodynamic response from visual cortex characterized by a rise at 3 s, peak activation at 5 s, and return to baseline by 10 s. We subtracted subjects' single-stimulus hemodynamic response from their paired-stimulus responses to isolate the contribution of the second stimulus. If the hemodynamic responses were fully additive, the residual should be a time-shifted replica of the single stimulus response. However, the amplitude of the hemodynamic response to the second checkerboard was smaller, and the peak latency was longer, than for the first. Furthermore, the amplitude decrement was dependent upon IPI, such that the response to the second stimulus at 1 s IPI was only 55% of that to a single stimulus, with recovery to 90% at a 6 s IPI. Peak latency was similarly dependent upon IPI with longer latencies observed for shorter IPIs. These results demonstrate an extended refractory period in the hemodynamic response to visual stimuli consistent with that shown previously for neuronal activity measured electrophysiologically.
A key emergent property of the primary visual cortex (V1) is the orientation selectivity of its neurons. The extent to which adult visual cortical neurons can exhibit changes in orientation selectivity is unknown. Here we use single-unit recording and intrinsic signal imaging in V1 of adult cats to demonstrate systematic repulsive shifts in orientation preference following short-term exposure (adaptation) to one stimulus orientation. In contrast to the common view of adaptation as a passive process by which responses around the adapting orientation are reduced, we show that changes in orientation tuning also occur due to response increases at orientations away from the adapting stimulus. Adaptation-induced orientation plasticity is thus an active time-dependent process that involves network interactions and includes both response depression and enhancement.
The linearity of the cerebral perfusion response relative to stimulus duration is an important consideration in the characterization of the relationship between regional cerebral blood flow (CBF), cerebral metabolism, and the blood oxygenation level dependent (BOLD) signal. It is also a critical component in the design and analysis of functional neuroimaging studies. To study the linearity of the CBF response to different duration stimuli, the perfusion response in primary motor and visual cortices was measured during stimulation using an arterial spin labeling technique with magnetic resonance imaging (MRI) that allows simultaneous measurement of CBF and BOLD changes. In each study, the perfusion response was measured for stimuli lasting 2, 6, and 18 sec. The CBF response was found in general to be nonlinearly related to stimulus duration, although the strength of nonlinearity varied between the motor and visual cortices. In contrast, the BOLD response was found to be strongly nonlinear in both regions studied, in agreement with previous findings. The observed nonlinearities are consistent with a model with a nonlinear step from stimulus to neural activity, a linear step from neural activity to CBF change, and a nonlinear step from CBF change to BOLD signal change.
The invariant properties of human cortical neurons cannot be studied directly by fMRI due to its limited spatial resolution. One voxel obtained from a fMRI scan contains several hundred thousands neurons. Therefore, the fMRI signal may average out a heterogeneous group of highly selective neurons. Here, we present a novel experimental paradigm for fMRI, functional magnetic resonance-adaptation (fMR-A), that enables to tag specific neuronal populations within an area and investigate their functional properties. This approach contrasts with conventional mapping methods that measure the averaged activity of a region. The application of fMR-A to study the functional properties of cortical neurons proceeds in two stages: First, the neuronal population is adapted by repeated presentation of a single stimulus. Second, some property of the stimulus is varied and the recovery from adaptation is assessed. If the signal remains adapted, it will indicate that the neurons are invariant to that attribute. However, if the fMRI signal will recover from the adapted state it would imply that the neurons are sensitive to the property that was varied. Here, an application of fMR-A for studying the invariant properties of high-order object areas (lateral occipital complex--LOC) to changes in object size, position, illumination and rotation is presented. The results show that LOC is less sensitive to changes in object size and position compared to changes of illumination and viewpoint. fMR-A can be extended to other neuronal systems in which adaptation is manifested and can be used with event-related paradigms as well. By manipulating experimental parameters and testing recovery from adaptation it should be possible to gain insight into the functional properties of cortical neurons which are beyond the spatial resolution limits imposed by conventional fMRI.