scholarly journals Level Dependence of Contextual Modulation in Auditory Cortex

2008 ◽  
Vol 99 (4) ◽  
pp. 1616-1627 ◽  
Author(s):  
Ben Scholl ◽  
Xiang Gao ◽  
Michael Wehr

Responses of cortical neurons to sensory stimuli within their receptive fields can be profoundly altered by the stimulus context. In visual and somatosensory cortex, contextual interactions have been shown to change sign from facilitation to suppression depending on stimulus strength. Contextual modulation of high-contrast stimuli tends to be suppressive, but for low-contrast stimuli tends to be facilitative. This trade-off may optimize contextual integration by cortical cells and has been suggested to be a general feature of cortical processing, but it remains unknown whether a similar phenomenon occurs in auditory cortex. Here we used whole cell and single-unit recordings to investigate how contextual interactions in auditory cortical neurons depend on the relative intensity of masker and probe stimuli in a two-tone stimulus paradigm. We tested the hypothesis that relatively low-level probes should show facilitation, whereas relatively high-level probes should show suppression. We found that contextual interactions were primarily suppressive across all probe levels, and that relatively low-level probes were subject to stronger suppression than high-level probes. These results were virtually identical for spiking and subthreshold responses. This suggests that, unlike visual cortical neurons, auditory cortical neurons show maximal suppression rather than facilitation for relatively weak stimuli.

2009 ◽  
Vol 102 (6) ◽  
pp. 3329-3339 ◽  
Author(s):  
Nima Mesgarani ◽  
Stephen V. David ◽  
Jonathan B. Fritz ◽  
Shihab A. Shamma

Population responses of cortical neurons encode considerable details about sensory stimuli, and the encoded information is likely to change with stimulus context and behavioral conditions. The details of encoding are difficult to discern across large sets of single neuron data because of the complexity of naturally occurring stimulus features and cortical receptive fields. To overcome this problem, we used the method of stimulus reconstruction to study how complex sounds are encoded in primary auditory cortex (AI). This method uses a linear spectro-temporal model to map neural population responses to an estimate of the stimulus spectrogram, thereby enabling a direct comparison between the original stimulus and its reconstruction. By assessing the fidelity of such reconstructions from responses to modulated noise stimuli, we estimated the range over which AI neurons can faithfully encode spectro-temporal features. For stimuli containing statistical regularities (typical of those found in complex natural sounds), we found that knowledge of these regularities substantially improves reconstruction accuracy over reconstructions that do not take advantage of this prior knowledge. Finally, contrasting stimulus reconstructions under different behavioral states showed a novel view of the rapid changes in spectro-temporal response properties induced by attentional and motivational state.


2008 ◽  
Vol 100 (2) ◽  
pp. 646-656 ◽  
Author(s):  
Ben Scholl ◽  
Michael Wehr

Sensory deafferentation results in rapid shifts in the receptive fields of cortical neurons, but the synaptic mechanisms underlying these changes remain unknown. The rapidity of these shifts has led to the suggestion that subthreshold inputs may be unmasked by a selective loss of inhibition. To study this, we used in vivo whole cell recordings to directly measure tone-evoked excitatory and inhibitory synaptic inputs in auditory cortical neurons before and after acoustic trauma. Here we report that acute acoustic trauma disrupted the balance of excitation and inhibition by selectively increasing and reducing the strength of inhibition at different positions within the receptive field. Inhibition was abolished for frequencies far below the trauma-tone frequency but was markedly enhanced near the edges of the region of elevated peripheral threshold. These changes occurred for relatively high-level tones. These changes in inhibition led to an expansion of receptive fields but not by a simple unmasking process. Rather, membrane potential responses were delayed and prolonged throughout the receptive field by distinct interactions between synaptic excitation and inhibition. Far below the trauma-tone frequency, decreased inhibition combined with prolonged excitation led to increased responses. Near the edges of the region of elevated peripheral threshold, increased inhibition served to delay rather than abolish responses, which were driven by prolonged excitation. These results show that the rapid receptive field shifts caused by acoustic trauma are caused by distinct mechanisms at different positions within the receptive field, which depend on differential disruption of excitation and inhibition.


2000 ◽  
Vol 84 (4) ◽  
pp. 2048-2062 ◽  
Author(s):  
Mitesh K. Kapadia ◽  
Gerald Westheimer ◽  
Charles D. Gilbert

To examine the role of primary visual cortex in visuospatial integration, we studied the spatial arrangement of contextual interactions in the response properties of neurons in primary visual cortex of alert monkeys and in human perception. We found a spatial segregation of opposing contextual interactions. At the level of cortical neurons, excitatory interactions were located along the ends of receptive fields, while inhibitory interactions were strongest along the orthogonal axis. Parallel psychophysical studies in human observers showed opposing contextual interactions surrounding a target line with a similar spatial distribution. The results suggest that V1 neurons can participate in multiple perceptual processes via spatially segregated and functionally distinct components of their receptive fields.


2020 ◽  
Author(s):  
Katherine C. Wood ◽  
Christopher F. Angeloni ◽  
Karmi Oxman ◽  
Claudia Clopath ◽  
Maria N. Geffen

SummaryLearning to avoid dangerous signals while preserving normal behavioral responses to safe stimuli is essential for everyday behavior and survival. Like other forms of learning, fear learning has a high level of inter-subject variability. Following an identical fear conditioning protocol, different subjects exhibit a range of fear specificity. Under high specificity, subjects specialize fear to only the paired (dangerous) stimulus, whereas under low specificity, subjects generalize fear to other (safe) sensory stimuli. Pathological fear generalization underlies emotional disorders, such as post-traumatic stress disorder. Despite decades of work, the neuronal basis that determines fear specificity level remains unknown. We identified the neuronal code that underlies variability in fear specificity. We performed longitudinal imaging of activity of neuronal ensembles in the auditory cortex of mice prior to and after the mice were subjected to differential fear conditioning. The neuronal code in the auditory cortex prior to learning predicted the level of specificity following fear learning across subjects. After fear learning, population neuronal responses were reorganized: the responses to the safe stimulus decreased, whereas the responses to the dangerous stimulus remained the same, rather than decreasing as in pseudo-conditioned subjects. The magnitude of these changes, however, did not correlate with learning specificity, suggesting that they did not reflect the fear memory. Together, our results identify a new, temporally restricted, function for cortical activity in associative learning. These results reconcile seemingly conflicting previous findings and provide for a neuronal code for determining individual patterns in learning.


2019 ◽  
Author(s):  
Baher A. Ibrahim ◽  
Caitlin Murphy ◽  
Guido Muscioni ◽  
Aynaz Taheri ◽  
Georgiy Yudintsev ◽  
...  

AbstractSince the discovery of the receptive field, scientists have tracked receptive field structure to gain insights about mechanisms of sensory processing. At the level of the thalamus and cortex, this linear filter approach has been challenged by findings that populations of cortical neurons respond in a stereotyped fashion to sensory stimuli. Here, we elucidate a possible mechanism by which gating of cortical representations occurs. All-or-none population responses (here called “ON” and “OFF” responses) were observed in vivo and in vitro in the mouse auditory cortex at near-threshold acoustic or electrical stimulation. ON-responses were associated with previously-described UP states in the auditory cortex. OFF-responses in the cortex were only eliminated by blocking GABAergic inhibition in the thalamus. Opto- and chemogenetic silencing of NTSR-positive corticothalamic layer 6 (CTL6) neurons as well as the pharmacological blocking of the thalamic reticular nucleus (TRN) retrieved the missing cortical responses, suggesting that the corticothalamic feedback inhibition via TRN controls the gating of thalamocortical activity. Moreover, the oscillation of the pre-stimulus activity of corticothalamic cells predicted the cortical ON vs. OFF responses, suggesting that underlying cortical oscillation controls thalamocortical gating. These data suggest that the thalamus may recruit cortical ensembles rather than linearly encoding ascending stimuli and that corticothalamic projections play a key role in selecting cortical ensembles for activation.


2006 ◽  
Vol 96 (1) ◽  
pp. 252-258 ◽  
Author(s):  
Rajiv Narayan ◽  
Gilberto Graña ◽  
Kamal Sen

Understanding how single cortical neurons discriminate between sensory stimuli is fundamental to providing a link between cortical neural responses and perception. The discrimination of sensory stimuli by cortical neurons has been intensively investigated in the visual and somatosensory systems. However, relatively little is known about discrimination of sounds by auditory cortical neurons. Auditory cortex plays a particularly important role in the discrimination of complex sounds, e.g., vocal communication sounds. The rich dynamic structure of such complex sounds on multiple time scales motivates two questions regarding cortical discrimination. How does discrimination depend on the temporal resolution of the cortical response? How does discrimination accuracy evolve over time? Here we investigate these questions in field L, the analogue of primary auditory cortex in zebra finches, analyzing temporal resolution and temporal integration in the discrimination of conspecific songs (songs of the bird's own species) for both anesthetized and awake subjects. We demonstrate the existence of distinct time scales for temporal resolution and temporal integration and explain how they arise from cortical neural responses to complex dynamic sounds.


2006 ◽  
Vol 96 (6) ◽  
pp. 2972-2983 ◽  
Author(s):  
Gabriel Soto ◽  
Nancy Kopell ◽  
Kamal Sen

Two fundamental issues in auditory cortical processing are the relative importance of thalamocortical versus intracortical circuits in shaping response properties in primary auditory cortex (ACx), and how the effects of neuromodulators on these circuits affect dynamic changes in network and receptive field properties that enhance signal processing and adaptive behavior. To investigate these issues, we developed a computational model of layers III and IV (LIII/IV) of AI, constrained by anatomical and physiological data. We focus on how the local and global cortical architecture shape receptive fields (RFs) of cortical cells and on how different well-established cholinergic effects on the cortical network reshape frequency-tuning properties of cells in ACx. We identify key thalamocortical and intracortical circuits that strongly affect tuning curves of model cortical neurons and are also sensitive to cholinergic modulation. We then study how differential cholinergic modulation of network parameters change the tuning properties of our model cells and propose two different mechanisms: one intracortical (involving muscarinic receptors) and one thalamocortical (involving nicotinic receptors), which may be involved in rapid plasticity in ACx, as recently reported in a study by Fritz and coworkers.


2016 ◽  
Author(s):  
Claudia Clopath ◽  
Tim P. Vogels ◽  
Robert C. Froemke ◽  
Henning Sprekeler

AbstractThe stimulus selectivity of synaptic currents in cortical neurons often shows a co-tuning of excitation and inhibition, but the mechanisms that underlie the emergence and plasticity of this co-tuning are not fully understood. Using a computational model, we show that an interaction of excitatory and inhibitory synaptic plasticity reproduces both the developmental and – when combined with a disinhibitory gate – the adult plasticity of excitatory and inhibitory receptive fields in auditory cortex. The co-tuning arises from inhibitory plasticity that balances excitation and inhibition, while excitatory stimulus selectivity can result from two different mechanisms. Inhibitory inputs with a broad stimulus tuning introduce a sliding threshold as in Bienenstock-Cooper-Munro rules, introducing an excitatory stimulus selectivity at the cost of a broader inhibitory receptive field. Alternatively, input asymmetries can be amplified by synaptic competition. The latter leaves any receptive field plasticity transient, a prediction we verify in recordings in auditory cortex.


2015 ◽  
Vol 112 (31) ◽  
pp. 9740-9744 ◽  
Author(s):  
Hiroshi Nomura ◽  
Kojiro Hara ◽  
Reimi Abe ◽  
Natsuko Hitora-Imamura ◽  
Ryota Nakayama ◽  
...  

Sensory stimuli not only activate specific populations of cortical neurons but can also silence other populations. However, it remains unclear whether neuronal silencing per se leads to memory formation and behavioral expression. Here we show that mice can report optogenetic inactivation of auditory neuron ensembles by exhibiting fear responses or seeking a reward. Mice receiving pairings of footshock and silencing of a neuronal ensemble exhibited a fear response selectively to the subsequent silencing of the same ensemble. The valence of the neuronal silencing was preserved for at least 30 d and was susceptible to extinction training. When we silenced an ensemble in one side of auditory cortex for conditioning, silencing of an ensemble in another side induced no fear response. We also found that mice can find a reward based on the presence or absence of the silencing. Neuronal silencing was stored as working memory. Taken together, we propose that neuronal silencing without explicit activation in the cerebral cortex is enough to elicit a cognitive behavior.


2016 ◽  
Author(s):  
Kei Majima ◽  
Paul Sukhanov ◽  
Tomoyasu Horikawa ◽  
Yukiyasu Kamitani

AbstractNeurons in high-level visual areas respond to more complex visual features with broader receptive fields (RFs) compared to those in low-level visual areas. Thus, high-level visual areas are generally considered to carry less information regarding the position of seen objects in the visual field. However, larger RFs may not imply loss of position information at the population level. Here, we evaluated how accurately the position of a seen object could be predicted (decoded) from activity patterns in each of six representative visual areas with different RF sizes (V1–V4, LOC, and FFA). We collected fMRI responses while human subjects viewed a ball randomly moving in a two-dimensional field. To estimate population RF sizes of individual fMRI voxels, RF models were fitted for individual voxels in each brain area. The voxels in higher visual areas showed larger estimated RFs than those in lower visual areas. Then, the ball’s position in a separate session was predicted by maximum likelihood regression (support vector regression, SVR) to predict the position. We found that regardless of the difference in RF size, all visual areas showed similar prediction accuracies, especially on the horizontal dimension. Higher areas showed slightly lower accuracies on the vertical dimension, which appears to be attributed to the narrower spatial distributions of the RFs centers. The results suggest that much of position information is preserved in population activity through the hierarchical visual pathway regardless of RF sizes, and is potentially available in later processing for recognition and behavior.Significance statementHigh-level ventral visual areas are thought to achieve position invariance with larger receptive fields at the cost of the loss of precise position information. However, larger receptive fields may not imply loss of position information at the population level. Here, multivoxel fMRI decoding reveals that high-level visual areas are predictive of an object’s position with similar accuracies to low-level visual areas, especially on the horizontal dimension, preserving the information potentially available for later processing.


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