
Manuel S MalmiercaUniversity of Salamanca · Instituto de Neurociencias de Castilla y León
Manuel S Malmierca
Doctor of Medicine
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137
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Publications (137)
Stimulus-specific adaptation (SSA) is a ubiquitous phenomenon in the animal kingdom across sensory modalities, but this type of neural response has rarely been studied using natural sounds in the auditory brain. Here, we leveraged the well-documented acoustic repertoire of the bat species Carollia perspicillata to study adaptation in the bat brain...
Mismatch negativity is an auditory-evoked biomarker for an array of neuropsychological disorders that occurs irrespective of consciousness, yet the generation mechanisms are still debated. Cortical slow oscillations occur during sleep or anesthesia and consist of reliable changes between “Up” and “Down” phases, characterised by high and low neural...
The neural mechanisms of novelty detection, especially in relation to behavior, are currently poorly understood. Here, we present a protocol for recording neuronal activity in macaque auditory cortex during novelty detection tasks. We describe steps for behavioral training, surgical headpost implantation, MRI-based electrode targeting, and electrop...
According to the predictive processing framework, perception emerges from the reciprocal exchange of predictions and prediction errors (PEs) between hierarchically organized neural circuits. The nonlemniscal division of the inferior colliculus (IC) is the earliest source of auditory PE signals, but their neuronal generators, properties, and functio...
Afferent inputs from the cochlea transmit auditory information to the central nervous system, where information is processed and passed up the hierarchy, ending in the auditory cortex. Through these brain pathways, spectral and temporal features of sounds are processed and sent to the cortex for perception. There are also many mechanisms in place f...
A fundamental property of sensory systems is their ability to detect novel stimuli in the ambient environment. The auditory brain contains neurons that decrease their response to repetitive sounds but increase their firing rate to novel or deviant stimuli; the difference between both responses is known as stimulus-specific adaptation or neuronal mi...
A fundamental property of sensory systems is their ability to detect novel stimuli in the ambient environment. The auditory brain contains neurons that decrease their response to repetitive sounds but increase their firing rate to novel or deviant stimuli; the difference between both responses is known as stimulus-specific adaptation or neuronal mi...
A fundamental property of sensory systems is their ability to detect novel stimuli in the environment. The auditory brain contains neurons that decrease their response to repetitive sounds but that increase their firing rate to novel or deviant stimuli; the difference between both responses is known as stimulus-specific adaptation or neuronal misma...
A fundamental property of sensory systems is their ability to detect novel stimuli in the environment. The auditory brain contains neurons that decrease their response to repetitive sounds but that increase their firing rate to novel or deviant stimuli; the difference between both responses is known as stimulus-specific adaptation or neuronal misma...
The relative importance or saliency of sensory inputs depend on the animal’s environmental context and the behavioural responses to these same inputs can vary over time. Here we show how freely moving rats, trained to discriminate between deviant tones embedded in a regular pattern of repeating stimuli and different variations of the classic oddbal...
A fundamental property of sensory systems is their ability to detect novel stimuli in the environment. The auditory brain contains neurons that decrease their response to repetitive sounds but that increase their firing rate to novel or deviant stimuli; the difference between both responses is known as stimulus-specific adaptation or neuronal misma...
Prediction provides key advantages for survival, and cognitive studies have demonstrated that the brain computes multilevel predictions. Evidence for predictions remains elusive at the neuronal level because of the complexity of separating neural activity into predictions and stimulus responses. We overcome this challenge by recording from single n...
The corticothalamic (CT) pathways emanate from either Layer 5 (L5) or 6 (L6) of the neocortex and largely outnumber the ascending, thalamocortical pathways. The CT pathways provide the anatomical foundations for an intricate, bidirectional communication between thalamus and cortex. They act as dynamic circuits of information transfer with the abili...
The auditory cortex (AC) encompasses distinct fields subserving partly different aspects of sound processing. One essential function of the AC is the detection of unpredicted sounds, as revealed by differential neural activity to predictable and unpredictable sounds. According to the predictive coding framework, this effect can be explained by repe...
The mismatch negativity (MMN) is a key biomarker of automatic deviance detection thought to emerge from 2 cortical sources. First, the auditory cortex (AC) encodes spectral regularities and reports frequency-specific deviances. Then, more abstract representations in the prefrontal cortex (PFC) allow to detect contextual changes of potential behavio...
Efficient sensory processing requires that the brain maximize its response to unexpected stimuli, while suppressing responsivity to expected events. Mismatch negativity (MMN) is an auditory event-related potential that occurs when a regular pattern is interrupted by an event that violates the expected properties of the pattern. According to the pre...
Dopamine guides behavior and learning through pleasure, according to classic understanding. Dopaminergic neurons are traditionally thought to signal positive or negative prediction errors (PEs) when reward expectations are, respectively, exceeded or not matched. These signed PEs are quite different from the unsigned PEs, which report surprise durin...
Auditory deviance detection is a function of the auditory system that allows reduction of the processing demand for repetitive stimuli while stressing unpredictable ones, which are potentially more informative. Deviance detection has been extensively studied in humans using the oddball paradigm, which evokes an event-related potential known as mism...
The inferior colliculus (IC) is an auditory structure where inputs from multiple lower centers converge, allowing the emergence of complex coding properties of auditory information such as stimulus-specific adaptation (SSA). SSA is the adaptation of neuronal responses to a specific repeated stimulus, which does not entirely generalize to other new...
Mismatch Negativity (MMN) is an electrophysiological signature that occurs in response to unexpected stimuli. It is often referred to as a measure of memory-based change detection, because the elicitation of a prediction error response relies on the formation of a prediction, which in turn, is dependent upon intact memory of previous auditory stimu...
Synopsis
A gentle introduction to the theoretical debate regarding pre-attentive auditory novelty processing and its two main biological signs: the mismatch negativity (MMN) and stimulus-specific adaptation (SSA). We present three conceptual frameworks: (1) the detection hypothesis, a cognitive account derived from the study of the MMN; (2) the ada...
Predictive coding theory describes perception as a hierarchical predictive model of sensation. Higher-level neural structures constrain the processing at lower-level structures by suppressing synaptic activity induced by predictable sensory input. But when predictions fail, deviant input is forwarded bottom-up as prediction error to update the perc...
According to predictive coding theory, perception emerges through the interplay of neural circuits that generate top-down predictions about environmental statistical regularities and those that generate bottom-up error signals to sensory deviations. Prediction error signals are hierarchically organized from subcortical structures to the auditory co...
The oddball paradigm has been widely exploited to study deviance detection. It serves to evaluate expectation, as it provokes an enhancement of the representation of a low-probability stimulus randomly intermingled in a sequence of frequent stimuli. We have previously used this paradigm to study stimulus-specific adaptation (SSA) in single unit rec...
Deviance detection is the automatic capacity to detect salient or novel stimuli within an otherwise monotonous acoustic environment. The neuronal substrate of deviance detection has been widely studied using the oddball paradigm, consisting on a sequence of repeated tones, referred to as standards, randomly interrupted by a low probability tone (th...
The oddball paradigm has been widely exploited to study deviance detection. It serves to evaluate expectation, as it provokes an enhancement of the representation of a low-probability stimulus randomly intermingled in a sequence of frequent stimuli. We have previously used this paradigm to study stimulus-specific adaptation (SSA) in single unit rec...
Efficient sensory processing requires that the brain is able to maximize its response to unexpected stimuli, while suppressing responsivity to expected events. Mismatch negativity (MMN) is an auditory event-related potential that occurs when a regular pattern is interrupted by an event that violates the expected properties of the pattern. MMN has b...
The Oxford Handbook of the Auditory Brainstem provides an in-depth reference to the organization and function of ascending and descending auditory pathways in the mammalian brainstem. Individual chapters are organized along the auditory pathway, beginning with the cochlea and ending with the auditory midbrain. Each chapter provides an introduction...
Neural responses to sensory inputs in a complex and natural environment must be weighted according to their relevance. To do so, the brain needs to be able to deal with sudden stimulus fluctuations in an ever-changing acoustic environment. Stimulus-specific adaptation (SSA) is a phenomenon of some neurons along the auditory pathway that show a redu...
In this review, we attempt to integrate the empirical evidence regarding stimulus-specific adaptation (SSA) and mismatch negativity (MMN) under a predictive coding perspective (also known as Bayesian or hierarchical-inference model). We propose a renewed methodology for SSA study, which enables a further decomposition of deviance detection into rep...
The inferior colliculus is a center of convergence for inhibitory and excitatory synaptic inputs that may be activated simultaneously by sound stimulation. Stimulus repetition may generate response habituation by changing the efficacy of neuron’s synaptic inputs. Specialized IC neurons reduce their response to repetitive tones, but restore their fi...
In this chapter, the neural circuitry of the inferior colliculus (IC) is described at a cellular level. The IC is subdivided into the central nucleus (ICC) and surrounding cortices that receive specific combinations of inputs and generate diverse outputs. Neuronal types in the IC can be distinguished by their dendritic arborization patterns, neuroc...
Stimulus-specific adaptation (SSA) is a special type of adaptation that allows
neurons to cease responding only to repetitive, background stimuli, while
preserving its responsiveness for other, new upcoming deviant stimuli. It
emerges subcortically in non-lemniscal neurons of the inferior colliculi,
propagating and evolving throughout the audit...
Perception is characterized by a reciprocal exchange of predictions and prediction error signals between neural regions. However, the relationship between such sensory mismatch responses and hierarchical predictive processing has not yet been demonstrated at the neuronal level in the auditory pathway. We recorded single-neuron activity from differe...
Cannabinoid receptors (CBRs) are widely distributed in the brain, including the inferior colliculus (IC). Here, we aim to study whether endocannabinoids influence a specific type of neuronal adaptation, namely, stimulus-specific adaptation (SSA) found in some IC neurons. SSA is important because it has been found as early as the level of the midbra...
Differences in the activity of neurotransmitters and neuromodulators, and consequently different neural responses, can be found between anesthetized and awake animals. Therefore, methods allowing the manipulation of synaptic systems in awake animals are required in order to determine the contribution of synaptic inputs to neuronal processing unaffe...
Electrophysiological and psychophysical responses to a low-intensity probe sound tend to be suppressed by a preceding high-intensity adaptor sound. Nevertheless, rare low-intensity deviant sounds presented among frequent high-intensity standard sounds in an intensity oddball paradigm can elicit an electroencephalographic mismatch negativity (MMN) r...
Author
Sensory systems automatically detect salient events in a monotonous ambient background. In humans, this change detection process is indexed by the mismatch negativity (MMN), a mid-late component of the auditory-evoked potentials that has become a central tool in cognitive and clinical neuroscience over the last 40 years. However, the neuron...
Selected dataset (SSA for the Nd and Pd components) reported in Results but not shown in any figure.
(XLSX)
Full dataset used in reported results and figures.
Organized into four spreadsheets: “Recording site,” list of all MUA recordings made, including those that didn’t show good responses to pure tones or otherwise could not be tested with the oddball paradigm; “Oddball (MUA),” list of all MUA recordings that could be tested with the oddball paradigm (...
Selected dataset (tone frequency, intensity, firing rate, and SI for each tone [f1 and f2, separately]) used to fit the linear model for the SI described in Results and to generate SI maps in Fig 6.
(XLSX)
Selected dataset used to generate the maps in Fig 4.
Contains separate spreadsheets for Fig 4A (map of CF, all recordings with a well-defined CF) and Fig 4B–4D (maps of adaptation, all recordings tested with the oddball paradigm).
(XLSX)
Average trial-by-trial spike counts used to fit the time course of SSA within each field and generate Fig 7.
(XLSX)
Selected dataset (amplitude and latency of the Nd and Pd difference) underlying barplots in Fig 8B.
(XLSX)
Selected dataset (full SSA index sample) underlying Fig 3.
(XLSX)
Selected dataset (CSI measures at different time windows) underlying boxplots and maps in Fig 5B and 5C.
(XLSX)
Although the scientific community appears to know a lot about MMN, about its neural generators and the computational processes that underlie its generation, do we have sufficient knowledge to understand what causes the reduction of MMN amplitude in schizophrenia? Here we attempt to integrate the evidence presented in this series of papers for the s...
Sequencing of the rat genome has allowed a better understanding of the rat physiology and biology, in turn promising to translate into a better understanding of human biology and disease processes, including neurobiology of hearing in humans. Sensory cells found in the organ of Corti are known as inner and outer hair cells; they have different func...
Unlabelled:
Neural encoding of an ever-changing acoustic environment is a complex and demanding process that depends on modulation by neuroactive substances. Some neurons of the inferior colliculus (IC) exhibit "stimulus-specific adaptation" (SSA), i.e., a decrease in their response to a repetitive sound, but not to a rare one. Previous studies ha...
In an ever changing auditory scene, change detection is an ongoing task performed by the auditory brain. Neurons in the midbrain and auditory cortex that exhibit stimulus-specific adaptation (SSA) may contribute to this process. Those neurons adapt to frequent sounds while retaining their excitability to rare sounds. Here, we test whether neurons e...
To follow an ever-changing auditory scene, the auditory brain is continuously creating a representation of the past to form expectations about the future. Unexpected events will produce an error in the predictions that should "trigger" the network's response. Indeed, neurons in the auditory midbrain, thalamus and cortex, respond to rarely occurring...
A remarkable ability of animals that is critical for survival is to detect and respond to to unexpected stimuli in an ever-changing world. Auditory neurons that show stimulus-specific adaptation (SSA), i.e., a decrease in their response to frequently occurring stimuli while maintaining responsiveness when different stimuli are presented, might part...
A unique aspect of the auditory system is the inferior colliculus (IC). This large midbrain structure serves as an obligatory synaptic station in both the ascending and descending auditory pathways. It has no equivalent in other sensory systems and it meets several unique needs of the auditory system. Most important, of course, is unifying the repr...
Rapid behavioral responses to unexpected events in the acoustic environment are critical for survival. Stimulus-specific adaptation (SSA) is the process whereby some auditory neurons respond better to rare stimuli than to repetitive stimuli. Most experiments on SSA have been performed under anesthesia, and it is unknown if SSA sensitivity is altere...
The ability to detect unexpected stimuli in the acoustic environment and determine their behavioral relevance to plan an appropriate reaction is critical for survival. This perspective article brings together several viewpoints and discusses current advances in understanding the mechanisms the auditory system implements to extract relevant informat...
The early stages of the auditory system need to preserve the timing information of sounds in order to extract the basic features of acoustic stimuli. At the same time, different processes of neuronal adaptation occur at several levels to further process the auditory information. For instance, auditory nerve fiber responses already experience adapta...
In this account, we attempt to integrate two parallel, but thus far, separate lines of research on auditory novelty detection: (1) human studies of EEG recordings of the mismatch negativity (MMN), and (2) animal studies of single-neuron recordings of stimulus-specific adaptation (SSA). The studies demonstrating the existence of novelty neurons show...
In the auditory brain, some populations of neurons exhibit stimulus-specific adaptation (SSA), whereby they adapt to frequently occurring stimuli but retain sensitivity to stimuli that are rare. SA has been observed in auditory structures from the midbrain to the primary auditory cortex (A1) and has been proposed to be a precursor to the generation...
Key points
Neurons in the medial geniculate body (MGB), the auditory thalamus, give stronger responses to rare sounds than to repetitive sounds, a phenomenon referred to as stimulus‐specific adaptation (SSA).
The present study sought to elucidate how the inhibitory thalamic circuitry acting at GABA A receptors affects the generation and/or modulati...
Deviancy detection in the continuous flow of sensory information into the central nervous system is of vital importance for animals. The task requires neuronal mechanisms that allow for an efficient representation of the environment by removing statistically redundant signals. Recently, the neuronal principles of auditory deviance detection have be...
Auditory neurons that exhibit stimulus-specific adaptation (SSA) decrease their response to common tones while retaining responsiveness to rare ones. We recorded single-unit responses from the inferior colliculus (IC) where SSA is known to occur and we explored for the first time SSA in the cochlear nucleus (CN) of rats. We assessed an important fu...
Stimulus-specific adaptation (SSA) is the ability of some neurons to respond better to rare than to frequent, repetitive stimuli. In the auditory system, SSA has been found at the level of the midbrain, thalamus, and cortex. While previous studies have used the whole overall neuronal response to characterize SSA, here we present a detailed analysis...
The ability to detect unexpected sounds within the environment is an important function of the auditory system, as a rapid response may be required for the organism to survive. Previous studies found a decreased response to repetitive stimuli (standard), but an increased response to rare or less frequent sounds (deviant) in individual neurons in th...
Many neurons in the central auditory pathway, from the inferior colliculus (IC) to the auditory cortex (AC), respond less strongly to a commonly occurring stimulus than one that rarely occurs. The origin of this phenomenon, called stimulus-specific adaptation (SSA), remains uncertain. The AC sends descending projections to the IC that terminate mos...
The ability to detect novel sounds in a complex acoustic context is crucial for survival. Neurons from midbrain through cortical levels adapt to repetitive stimuli, while maintaining responsiveness to rare stimuli, a phenomenon called stimulus-specific adaptation (SSA). The site of origin and mechanism of SSA are currently unknown. We used microion...
This chapter highlights the functional organization of the mouse auditory system and focuses on mouse as a useful and economical animal model for hearing research. Advances in gene targeting have led to a renaissance in the use of the mouse as a model for investigation of human disease mechanisms. Until recently, the most commonly used experimental...