Publications (41)291.8 Total impact
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Article: Analysis of slow (theta) oscillations as a potential temporal reference frame for information coding in sensory cortices.
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ABSTRACT: While sensory neurons carry behaviorally relevant information in responses that often extend over hundreds of milliseconds, the key units of neural information likely consist of much shorter and temporally precise spike patterns. The mechanisms and temporal reference frames by which sensory networks partition responses into these shorter units of information remain unknown. One hypothesis holds that slow oscillations provide a network-intrinsic reference to temporally partitioned spike trains without exploiting the millisecond-precise alignment of spikes to sensory stimuli. We tested this hypothesis on neural responses recorded in visual and auditory cortices of macaque monkeys in response to natural stimuli. Comparing different schemes for response partitioning revealed that theta band oscillations provide a temporal reference that permits extracting significantly more information than can be obtained from spike counts, and sometimes almost as much information as obtained by partitioning spike trains using precisely stimulus-locked time bins. We further tested the robustness of these partitioning schemes to temporal uncertainty in the decoding process and to noise in the sensory input. This revealed that partitioning using an oscillatory reference provides greater robustness than partitioning using precisely stimulus-locked time bins. Overall, these results provide a computational proof of concept for the hypothesis that slow rhythmic network activity may serve as internal reference frame for information coding in sensory cortices and they foster the notion that slow oscillations serve as key elements for the computations underlying perception.PLoS Computational Biology 10/2012; 8(10):e1002717. · 5.22 Impact Factor -
Article: A precluding but not ensuring role of entrained low-frequency oscillations for auditory perception.
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ABSTRACT: Oscillatory activity in sensory cortices reflects changes in local excitation-inhibition balance, and recent work suggests that phase signatures of ongoing oscillations predict the perceptual detection of subsequent stimuli. Low-frequency oscillations are also entrained by dynamic natural scenes, suggesting that the chance of detecting a brief target depends on the relative timing of this to the entrained rhythm. We tested this hypothesis in humans by implementing a cocktail-party-like scenario requiring subjects to detect a target embedded in a cacophony of background sounds. Using EEG to measure auditory cortical oscillations, we find that the chance of target detection systematically depends on both power and phase of theta-band (2-6 Hz) but not alpha-band (8-12 Hz) oscillations before target. Detection rates were higher and responses faster when oscillatory power was low and both detection rate and response speed were modulated by phase. Intriguingly, the phase dependency was stronger for miss than for hit trials, suggesting that phase has a inhibiting but not ensuring role for detection. Entrainment of theta range oscillations prominently occurs during the processing of attended complex stimuli, such as vocalizations and speech. Our results demonstrate that this entrainment to attended sensory environments may have negative effects on the detection of individual tokens within the environment, and they support the notion that specific phase ranges of cortical oscillations act as gatekeepers for perception.Journal of Neuroscience 08/2012; 32(35):12268-76. · 7.11 Impact Factor -
Article: Neurons with stereotyped and rapid responses provide a reference frame for relative temporal coding in primate auditory cortex.
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ABSTRACT: The precise timing of spikes of cortical neurons relative to stimulus onset carries substantial sensory information. To access this information the sensory systems would need to maintain an internal temporal reference that reflects the precise stimulus timing. Whether and how sensory systems implement such reference frames to decode time-dependent responses, however, remains debated. Studying the encoding of naturalistic sounds in primate (Macaca mulatta) auditory cortex we here investigate potential intrinsic references for decoding temporally precise information. Within the population of recorded neurons, we found one subset responding with stereotyped fast latencies that varied little across trials or stimuli, while the remaining neurons had stimulus-modulated responses with longer and variable latencies. Computational analysis demonstrated that the neurons with stereotyped short latencies constitute an effective temporal reference for relative coding. Using the response onset of a simultaneously recorded stereotyped neuron allowed decoding most of the stimulus information carried by onset latencies and the full spike train of stimulus-modulated neurons. Computational modeling showed that few tens of such stereotyped reference neurons suffice to recover nearly all information that would be available when decoding the same responses relative to the actual stimulus onset. These findings reveal an explicit neural signature of an intrinsic reference for decoding temporal response patterns in the auditory cortex of alert animals. Furthermore, they highlight a role for apparently unselective neurons as an early saliency signal that provides a temporal reference for extracting stimulus information from other neurons.Journal of Neuroscience 02/2012; 32(9):2998-3008. · 7.11 Impact Factor -
Article: Suppressive competition: how sounds may cheat sight.
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ABSTRACT: In this issue of Neuron, Iurilli et al. (2012) demonstrate that auditory cortex activation directly engages local GABAergic circuits in V1 to induce sound-driven hyperpolarizations in layer 2/3 and layer 6 pyramidal neurons. Thereby, sounds can directly suppress V1 activity and visual driven behavior.Neuron 02/2012; 73(4):627-9. · 14.74 Impact Factor -
Article: EEG Phase Patterns Reflect the Selectivity of Neural Firing.
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ABSTRACT: Oscillations are pervasive in encephalographic signals and supposedly reflect cognitive processes and sensory representations. While the relation between oscillation amplitude (power) and sensory-cognitive variables has been extensively studied, recent work reveals that the dynamic oscillation signature (phase pattern) can carry information about such processes to a greater degree than amplitude. To elucidate the neural correlates of oscillatory phase patterns, we compared the stimulus selectivity of neural firing rates and auditory-driven electroencephalogram (EEG) oscillations. We employed the same naturalistic sound stimuli in 2 experiments, one recording scalp EEGs in humans and one recording intracortical local field potentials (LFPs) and single neurons in macaque auditory cortex. Using stimulus decoding techniques, we show that stimulus selective firing patterns imprint on the phase rather than the amplitude of slow (theta band) oscillations in LFPs and EEG. In particular, we find that stimuli which can be discriminated by firing rates can also be discriminated by phase patterns but not by oscillation amplitude and that stimulus-specific phase patterns also persist in the absence of increases of oscillation power. These findings support a neural basis for stimulus selective and entrained EEG phase patterns and reveal a level of interrelation between encephalographic signals and neural firing beyond simple amplitude covariations in both signals.Cerebral Cortex 02/2012; · 6.54 Impact Factor -
Article: Voice cells in the primate temporal lobe.
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ABSTRACT: Communication signals are important for social interactions and survival and are thought to receive specialized processing in the visual and auditory systems. Whereas the neural processing of faces by face clusters and face cells has been repeatedly studied [1-5], less is known about the neural representation of voice content. Recent functional magnetic resonance imaging (fMRI) studies have localized voice-preferring regions in the primate temporal lobe [6, 7], but the hemodynamic response cannot directly assess neurophysiological properties. We investigated the responses of neurons in an fMRI-identified voice cluster in awake monkeys, and here we provide the first systematic evidence for voice cells. "Voice cells" were identified, in analogy to "face cells," as neurons responding at least 2-fold stronger to conspecific voices than to "nonvoice" sounds or heterospecific voices. Importantly, whereas face clusters are thought to contain high proportions of face cells [4] responding broadly to many faces [1, 2, 4, 5, 8-10], we found that voice clusters contain moderate proportions of voice cells. Furthermore, individual voice cells exhibit high stimulus selectivity. The results reveal the neurophysiological bases for fMRI-defined voice clusters in the primate brain and highlight potential differences in how the auditory and visual systems generate selective representations of communication signals.Current biology: CB 08/2011; 21(16):1408-15. · 10.99 Impact Factor -
Article: Local field potential phase and spike timing convey information about different visual features in primary visual cortex
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ABSTRACT: The natural visual environment is characterized by both "what/where" aspects (image features such as contrast or orientation which are defined by the relationship between visual signals simultaneously presented at different points in space) and "when" aspects, describing the temporal variations of the image features. Both "when" and "what/ where" information is necessary to describe and under-stand the natural visual environment, and to take appro-priate behavioral decisions. While "where" can be considered embedded as retinotopy, it is likely that loca-lized neural populations in the visual cortex keep a simultaneous representation of both "what" and "when" aspects of the visual stimuli. However, little is yet known about how the spike trains of neurons in primary visual cortex encode both sources of information. The traditional hypothesis in systems neuroscience is that sensory variables are represented by a rate code, i.e. all sensory information is encoded by the number of spikes emitted over relatively long time windows. Although the relevance of rate in encoding static features is well established, this code can be inherently ambiguous in changing environments [1] and it is unlikely that this code is rich enough to represent simultaneously different types of information. Therefore here we explore the hypothesis that the timing of spikes is a crucial variable in representing both "what" and "when" aspects of the natural visual environment. To address these issues, we recorded single unit activity and LFPs in primary visual cortex of opiate anaesthetized macaques during the binocular presentation of naturalistic color movies. By means of computational analysis, we extracted several image features (color, orientation, lumi-nance, space and time contrast, motion) from the recep-tive fields of each single neuron. We then considered two different spike timing codes previously studied in both the auditory [2] and the visual cortex [3]. In the first code, which we call spike patterns code, sequences of spike times from single neurons are measured (with a resolution of the order of 10 ms) with respect to the time course of the external stimulus. In the second code, which we call phase of firing code, spikes are measured with respect to the phase of the concurrent low frequency LFPs recorded from the same electrode as the spikes. We then used these data to investigate systematically which types of neural codes carry information about the static features of the image and which neural codes carry information about the time course of these features. We found that both "when" and "what" aspects are encoded simultaneously by spike times of visual cortical neurons. However, "what" and "when" are encoded by two different neural information streams; "what" aspects are encoded (on a fine scale of few ms) by spike patterns, and "when" stimulus aspects are encoded by the phase of firing (on a coarse scale of hundreds of ms).08/2011; -
Article: Does the information in the phase of low frequency LFP reflect the low frequency envelope of local spike rates?
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ABSTRACT: Recently, it has been shown that when the timing of spikes is measured relative to the phase of the cortical local field potentials (LFP), spikes can carry substantial more information about an external stimulus [1]. Experimental studies in sensory cortices of macaque have shown that the extra information obtained with such phase-of-firing codes above that in the firing rate alone ranges from 55% in primary visual cortex [1] to more than 100% in primary auditory cortex [2]. Here, we use a mathematical model that relates local spike trains and the resulting LFP, to explain the emergence of the phase-of-firing codes in cortex. The model is based on the one proposed in [3] and incorporates two types of integration over the spiking activity: i) a time convolution that results from the filtering properties of neural structures [4], which embeds history effects in LFP from past spiking activity, and ii) an integration step over the activity of neurons in the neighbourhood of the measuring electrode. When the spikes recorded from macaque primary visual cortex were used to synthesize the LFP, the model could reproduce the phase-of-firing information found using the real LFP, as shown in Figure 1. This suggests that an important component of phase-of-firing information originates from the surrounding neural population and past spiking activity. The next question that arises is what is the relative contribution of the neuron population size and the length of the firing rate history embedded in the LFP. We are currently investigating this question by parametrically varying both the population size and time integration ranges in generating the synthetic LFP. Figure 1. Comparison of the phase-of-firing information using synthetic and real LFP. The original data corresponds to LFP and spiking activity from 78 recordings channels in macaque V1, obtained while the animals were presented a movie [1]. A. Information in the phase-of-firing code as a function of the LFP frequency band (black dots, with error bars indicating SEM over the dataset), and in the spike count (dashed line, with SEM indicated by grey area). In this panel, the LFP was simulated using real spikes with a mathematical model based on the one in [3]. B. As in A, however in this case both spikes and LFP correspond to real data [1].BMC Neuroscience 07/2011; 12:227. · 3.04 Impact Factor -
Article: Millisecond encoding precision of auditory cortex neurons.
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ABSTRACT: Neurons in auditory cortex are central to our perception of sounds. However, the underlying neural codes, and the relevance of millisecond-precise spike timing in particular, remain debated. Here, we addressed this issue in the auditory cortex of alert nonhuman primates by quantifying the amount of information carried by precise spike timing about complex sounds presented for extended periods of time (random tone sequences and natural sounds). We investigated the dependence of stimulus information on the temporal precision at which spike times were registered and found that registering spikes at a precision coarser than a few milliseconds significantly reduced the encoded information. This dependence demonstrates that auditory cortex neurons can carry stimulus information at high temporal precision. In addition, we found that the main determinant of finely timed information was rapid modulation of the firing rate, whereas higher-order correlations between spike times contributed negligibly. Although the neural coding precision was high for random tone sequences and natural sounds, the information lost at a precision coarser than a few milliseconds was higher for the stimulus sequence that varied on a faster time scale (random tones), suggesting that the precision of cortical firing depends on the stimulus dynamics. Together, these results provide a neural substrate for recently reported behavioral relevance of precisely timed activity patterns with auditory cortex. In addition, they highlight the importance of millisecond-precise neural coding as general functional principle of auditory processing--from the periphery to cortex.Proceedings of the National Academy of Sciences 09/2010; 107(39):16976-81. · 9.68 Impact Factor -
Article: Unimodal responses prevail within the multisensory claustrum.
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ABSTRACT: The claustrum receives afferent inputs from multiple sensory-related brain areas, prompting speculation about a role in integrating information across sensory modalities. Here we directly test this hypothesis by probing neurons in the primate claustrum for functional characteristics of multisensory processing. To this end we recorded neuronal responses to naturalistic audio-visual stimuli from the claustra of alert monkeys. Our results reveal the existence of distinct claustral zones comprised of unimodal neurons associated with the auditory and visual modalities. In a visual zone within the ventral claustrum neurons responded to visual stimuli but not to sounds, whereas in an auditory zone located within the central claustrum neurons responded to sounds but not to visual stimuli. Importantly, we find that neurons within either zone are not influenced by stimuli in the other modality and do not exhibit the typical response characteristics usually associated with multisensory processing. While these results confirm the notion of the claustrum as a multisensory structure per se, they argue against the hypothesis of the claustrum serving as an integrator of sensory information.Journal of Neuroscience 09/2010; 30(39):12902-7. · 7.11 Impact Factor -
Article: The multisensory nature of unisensory cortices: a puzzle continued.
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ABSTRACT: Multisensory integration is central to perception, and recent work drafts it as a distributed process involving many and even primary sensory cortices. Studies in behaving animals performing a multisensory task provide an ideal means to elucidate the underlying neural basis, and a new study by Lemus et al. in this issue of Neuron thrusts in this direction.Neuron 07/2010; 67(2):178-80. · 14.74 Impact Factor -
Article: Complex times for earthquakes, stocks, and the brain's activity.
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ABSTRACT: A new study by He et al. in this issue of Neuron shows that large-scale arrhythmic (1/f) brain activity contains nested temporal structure in the form of crossfrequency coupling. This suggests temporal organization in neural mass activity beyond oscillations and draws attention to ubiquitous but often ignored arrhythmic patterns in neural activity.Neuron 05/2010; 66(3):329-31. · 14.74 Impact Factor -
Article: Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands.
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ABSTRACT: Studies analyzing sensory cortical processing or trying to decode brain activity often rely on a combination of different electrophysiological signals, such as local field potentials (LFPs) and spiking activity. Understanding the relation between these signals and sensory stimuli and between different components of these signals is hence of great interest. We here provide an analysis of LFPs and spiking activity recorded from visual and auditory cortex during stimulation with natural stimuli. In particular, we focus on the time scales on which different components of these signals are informative about the stimulus, and on the dependencies between different components of these signals. Addressing the first question, we find that stimulus information in low frequency bands (<12 Hz) is high, regardless of whether their energy is computed at the scale of milliseconds or seconds. Stimulus information in higher bands (>50 Hz), in contrast, is scale dependent, and is larger when the energy is averaged over several hundreds of milliseconds. Indeed, combined analysis of signal reliability and information revealed that the energy of slow LFP fluctuations is well related to the stimulus even when considering individual or few cycles, while the energy of fast LFP oscillations carries information only when averaged over many cycles. Addressing the second question, we find that stimulus information in different LFP bands, and in different LFP bands and spiking activity, is largely independent regardless of time scale or sensory system. Taken together, these findings suggest that different LFP bands represent dynamic natural stimuli on distinct time scales and together provide a potentially rich source of information for sensory processing or decoding brain activity.Journal of Computational Neuroscience 03/2010; 29(3):533-45. · 2.51 Impact Factor -
Article: Sensory neural codes using multiplexed temporal scales.
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ABSTRACT: Determining how neuronal activity represents sensory information is central for understanding perception. Recent work shows that neural responses at different timescales can encode different stimulus attributes, resulting in a temporal multiplexing of sensory information. Multiplexing increases the encoding capacity of neural responses, enables disambiguation of stimuli that cannot be discriminated at a single response timescale, and makes sensory representations stable to the presence of variability in the sensory world. Thus, as we discuss here, temporal multiplexing could be a key strategy used by the brain to form an information-rich and stable representation of the environment.Trends in Neurosciences 03/2010; 33(3):111-20. · 14.23 Impact Factor -
Article: Coupling of neural activity and fMRI-BOLD in the motion area MT.
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ABSTRACT: The fMRI-BOLD contrast is widely used to study the neural basis of sensory perception and cognition. This signal, however, reflects neural activity only indirectly, and the detailed mechanisms of neurovascular coupling and the neurophysiological correlates of the BOLD signal remain debated. Here we investigate the coupling of BOLD and electrophysiological signals in the motion area MT of the macaque monkey by simultaneously recording both signals. Our results demonstrate that a prominent neuronal response property of area MT, so-called motion opponency, can be used to induce dissociations of BOLD and neuronal firing. During the presentation of a stimulus optimally driving the local neurons, both field potentials [local field potentials (LFPs)] and spiking activity [multi-unit activity (MUA)] correlated with the BOLD signal. When introducing the motion opponency stimulus, however, correlations of MUA with BOLD were much reduced, and LFPs were a much better predictor of the BOLD signal than MUA. In addition, for a subset of recording sites we found positive BOLD and LFP responses in the presence of decreases in MUA, regardless of the stimulus used. Together, these results demonstrate that correlations between BOLD and MUA are dependent on the particular site and stimulus paradigm, and foster the notion that the fMRI-BOLD signal reflects local dendrosomatic processing and synaptic activity rather than principal neuron spiking responses.Magnetic Resonance Imaging 02/2010; 28(8):1087-94. · 1.99 Impact Factor -
Article: Visual enhancement of the information representation in auditory cortex.
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ABSTRACT: Combining information across different sensory modalities can greatly facilitate our ability to detect, discriminate, or recognize sensory stimuli. Although this process of sensory integration has usually been attributed to classical association cortices, recent work has demonstrated that neuronal activity in early sensory cortices can also be influenced by cross-modal inputs. Here we demonstrate that such "early" multisensory influences enhance the information carried by neurons about multisensory stimuli. By recording in auditory cortex of alert monkeys watching naturalistic audiovisual stimuli, we quantified the effect of visual influences on the trial-to-trial response variability and on the amount of information carried by neural responses. We found that firing rates and precisely timed spike patterns of individual units became more reliable across trials and time when multisensory stimuli were presented, leading to greater encoded stimulus information. Importantly, this multisensory information enhancement was much reduced when the visual stimulus did not match the sound. These results demonstrate that multisensory influences enhance information processing already at early stages in cortex, suggesting that sensory integration is a distributed process, commencing in lower sensory areas and continuing in higher association cortices.Current biology: CB 01/2010; 20(1):19-24. · 10.99 Impact Factor -
Article: Modulation of visual responses in the superior temporal sulcus by audio-visual congruency.
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ABSTRACT: Our ability to identify or recognize visual objects is often enhanced by evidence provided by other sensory modalities. Yet, where and how visual object processing benefits from the information received by the other senses remains unclear. One candidate region is the temporal lobe, which features neural representations of visual objects, and in which previous studies have provided evidence for multisensory influences on neural responses. In the present study we directly tested whether visual representations in the lower bank of the superior temporal sulcus (STS) benefit from acoustic information. To this end, we recorded neural responses in alert monkeys passively watching audio-visual scenes, and quantified the impact of simultaneously presented sounds on responses elicited by the presentation of naturalistic visual scenes. Using methods of stimulus decoding and information theory, we then asked whether the responses of STS neurons become more reliable and informative in multisensory contexts. Our results demonstrate that STS neurons are indeed sensitive to the modality composition of the sensory stimulus. Importantly, information provided by STS neurons' responses about the particular visual stimulus being presented was highest during congruent audio-visual and unimodal visual stimulation, but was reduced during incongruent bimodal stimulation. Together, these findings demonstrate that higher visual representations in the STS not only convey information about the visual input but also depend on the acoustic context of a visual scene.Frontiers in Integrative Neuroscience 01/2010; 4:10. -
Chapter: The Electrophysiological Background of the fMRI Signal
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ABSTRACT: The ability to non-invasively study the architecture and function of the human brain constitutes one of the most exciting cornerstones for modern medicine, psychology and neuroscience. Current in vivo imaging techniques not only provide clinically essential information and allow new forms of treatment, but also reveal insights into the mechanisms behind brain function and malfunction. This supremacy of modern imaging rests on its ability to study the structural properties of the nervous system simultaneously with the functional changes related to neuronal activity. As a result, imaging allows us to combine information about the spatial organization and connectivity of the nervous system with information about the underlying neuronal processes and provides the only means to link perception and cognition with the neural substrates in the human brain.12/2009: pages 23-33; -
Article: Phase resetting as a mechanism for supramodal attentional control.
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ABSTRACT: Attentional modulation and cross-modal integration might partly rely on the same neurophysiological mechanisms. As a new study by Lakatos et al. in this issue of Neuron shows, attended stimuli in one sensory modality not only modulate oscillatory activity within the primary cortex of the same modality but also reset the phase of ongoing oscillations in primary cortices of other modalities.Neuron 11/2009; 64(3):300-2. · 14.74 Impact Factor -
Article: Monkey drumming reveals common networks for perceiving vocal and nonvocal communication sounds.
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ABSTRACT: Salient sounds such as those created by drumming can serve as means of nonvocal acoustic communication in addition to vocal sounds. Despite the ubiquity of drumming across human cultures, its origins and the brain regions specialized in processing such signals remain unexplored. Here, we report that an important animal model for vocal communication, the macaque monkey, also displays drumming behavior, and we exploit this finding to show that vocal and nonvocal communication sounds are represented by overlapping networks in the brain's temporal lobe. Observing social macaque groups, we found that these animals use artificial objects to produce salient periodic sounds, similar to acoustic gestures. Behavioral tests confirmed that these drumming sounds attract the attention of listening monkeys similarly as conspecific vocalizations. Furthermore, in a preferential looking experiment, drumming sounds influenced the way monkeys viewed their conspecifics, suggesting that drumming serves as a multimodal signal of social dominance. Finally, by using high-resolution functional imaging we identified those brain regions preferentially activated by drumming sounds or by vocalizations and found that the representations of both these communication sounds overlap in caudal auditory cortex and the amygdala. The similar behavioral responses to drumming and vocal sounds, and their shared neural representation, suggest a common origin of primate vocal and nonvocal communication systems and support the notion of a gestural origin of speech and music.Proceedings of the National Academy of Sciences 10/2009; 106(42):18010-5. · 9.68 Impact Factor
Top co-authors
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Institutions
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2005–2012
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Max-Planck-Institut für biologische Kybernetik
- Abteilung für Physiologie Kognitiver Prozesse
Tübingen, Baden-Wuerttemberg, Germany
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2010
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Italian Institute of Technology (IIT)
- Department of Robotics, Brain and Cognitive Sciences
Genova, Liguria, Italy
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