scholarly journals Synthesis of a comprehensive population code for contextual features in the awake sensory cortex

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Evan H Lyall ◽  
Daniel P Mossing ◽  
Scott R Pluta ◽  
Yun Wen Chu ◽  
Amir Dudai ◽  
...  

How cortical circuits build representations of complex objects is poorly understood. Individual neurons must integrate broadly over space, yet simultaneously obtain sharp tuning to specific global stimulus features. Groups of neurons identifying different global features must then assemble into a population that forms a comprehensive code for these global stimulus properties. Although the logic for how single neurons summate over their spatial inputs has been well-explored in anesthetized animals, how large groups of neurons compose a flexible population code of higher order features in awake animals is not known. To address this question, we probed the integration and population coding of higher order stimuli in the somatosensory and visual cortices of awake mice using two-photon calcium imaging across cortical layers. We developed a novel tactile stimulator that allowed the precise measurement of spatial summation even in actively whisking mice. Using this system, we found a sparse but comprehensive population code for higher order tactile features that depends on a heterogeneous and neuron-specific logic of spatial summation beyond the receptive field. Different somatosensory cortical neurons summed specific combinations of sensory inputs supra-linearly, but integrated other inputs sub-linearly, leading to selective responses to higher order features. Visual cortical populations employed a nearly identical scheme to generate a comprehensive population code for contextual stimuli. These results suggest that a heterogeneous logic of input-specific supra-linear summation may represent a widespread cortical mechanism for the synthesis of sparse higher order feature codes in neural populations. This may explain how the brain exploits the thalamocortical expansion of dimensionality to encode arbitrary complex features of sensory stimuli.

2020 ◽  
Author(s):  
Evan H. Lyall ◽  
Daniel P. Mossing ◽  
Scott R. Pluta ◽  
Amir Dudai ◽  
Hillel Adesnik

AbstractHow cortical circuits build representations of complex objects is poorly understood. The massive dimensional expansion from the thalamus to the primary sensory cortex may enable sparse, comprehensive representations of higher order features to facilitate object identification. To generate such a code, cortical neurons must integrate broadly over space, yet simultaneously obtain sharp tuning to specific stimulus features. The logic of cortical integration that may synthesize such a sparse, high dimensional code for complex features is not known. To address this question, we probed the integration and population coding of higher order stimuli in the somatosensory and visual cortices of awake mice using two-photon calcium imaging across cortical layers. We found that somatosensory and visual cortical neurons sum highly specific combinations of sensory inputs supra-linearly, but integrate other inputs sub-linearly, leading to selective responses to higher order features. This integrative process generates a sparse, but comprehensive code for complex stimuli from the earliest stages of cortical processing. These results from multiple sensory modalities imply that input-specific supra-linear summation may represent a widespread cortical mechanism for the synthesis of higher order feature codes. This new mechanism may explain how the brain exploits the thalamocortical expansion of dimensionality to encode arbitrary complex features of sensory stimuli.


2006 ◽  
Vol 18 (7) ◽  
pp. 1555-1576 ◽  
Author(s):  
Marcelo A. Montemurro ◽  
Stefano Panzeri

We study the relationship between the accuracy of a large neuronal population in encoding periodic sensory stimuli and the width of the tuning curves of individual neurons in the population. By using general simple models of population activity, we show that when considering one or two periodic stimulus features, a narrow tuning width provides better population encoding accuracy. When encoding more than two periodic stimulus features, the information conveyed by the population is instead maximal for finite values of the tuning width. These optimal values are only weakly dependent on model parameters and are similar to the width of tuning to orientation ormotion direction of real visual cortical neurons. A very large tuning width leads to poor encoding accuracy, whatever the number of stimulus features encoded. Thus, optimal coding of periodic stimuli is different from that of nonperiodic stimuli, which, as shown in previous studies, would require infinitely large tuning widths when coding more than two stimulus features.


2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Jermyn Z. See ◽  
Natsumi Y. Homma ◽  
Craig A. Atencio ◽  
Vikaas S. Sohal ◽  
Christoph E. Schreiner

AbstractNeuronal activity in auditory cortex is often highly synchronous between neighboring neurons. Such coordinated activity is thought to be crucial for information processing. We determined the functional properties of coordinated neuronal ensembles (cNEs) within primary auditory cortical (AI) columns relative to the contributing neurons. Nearly half of AI cNEs showed robust spectro-temporal receptive fields whereas the remaining cNEs showed little or no acoustic feature selectivity. cNEs can therefore capture either specific, time-locked information of spectro-temporal stimulus features or reflect stimulus-unspecific, less-time specific processing aspects. By contrast, we show that individual neurons can represent both of those aspects through membership in multiple cNEs with either high or absent feature selectivity. These associations produce functionally heterogeneous spikes identifiable by instantaneous association with different cNEs. This demonstrates that single neuron spike trains can sequentially convey multiple aspects that contribute to cortical processing, including stimulus-specific and unspecific information.


eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Bram-Ernst Verhoef ◽  
John HR Maunsell

Shifting attention among visual stimuli at different locations modulates neuronal responses in heterogeneous ways, depending on where those stimuli lie within the receptive fields of neurons. Yet how attention interacts with the receptive-field structure of cortical neurons remains unclear. We measured neuronal responses in area V4 while monkeys shifted their attention among stimuli placed in different locations within and around neuronal receptive fields. We found that attention interacts uniformly with the spatially-varying excitation and suppression associated with the receptive field. This interaction explained the large variability in attention modulation across neurons, and a non-additive relationship among stimulus selectivity, stimulus-induced suppression and attention modulation that has not been previously described. A spatially-tuned normalization model precisely accounted for all observed attention modulations and for the spatial summation properties of neurons. These results provide a unified account of spatial summation and attention-related modulation across both the classical receptive field and the surround.


2020 ◽  
Author(s):  
Jason Alipio ◽  
Catherine Haga ◽  
Megan E Fox ◽  
Keiko Arakawa ◽  
Rakshita Balaji ◽  
...  

One consequence of the opioid epidemic are lasting neurodevelopmental sequelae afflicting adolescents exposed to opioids in the womb. A translationally relevant and developmentally accurate preclinical model is needed to understand the behavioral, circuit, network, and molecular abnormalities resulting from this exposure. By employing a novel preclinical model of perinatal fentanyl exposure, our data reveal that fentanyl has several dose-dependent, developmental consequences to somatosensory function and behavior. Newborn male and female mice exhibit signs of withdrawal and sensory-related deficits that extend at least to adolescence. As fentanyl exposure does not affect dams' health or maternal behavior, these effects result from the direct actions of perinatal fentanyl on the pups' developing brain. At adolescence, exposed mice exhibit reduced adaptation to sensory stimuli, and a corresponding impairment in primary somatosensory (S1) function. In vitro electrophysiology demonstrates a long-lasting reduction in S1 synaptic excitation, evidenced by decreases in release probability, NMDA receptor-mediated postsynaptic currents, and frequency of miniature excitatory postsynaptic currents, as well as increased frequency of miniature inhibitory postsynaptic currents. In contrast, anterior cingulate cortical neurons exhibit an opposite phenotype, with increased synaptic excitation. Consistent with these changes, electrocorticograms reveal suppressed ketamine-evoked γ oscillations. Morphological analysis of S1 pyramidal neurons indicate reduced dendritic complexity, dendritic length, and soma size. Further, exposed mice exhibited abnormal cortical mRNA expression of key receptors and neuronal growth and development, changes that were consistent with the electrophysiological and morphological changes. These findings demonstrate the lasting sequelae of perinatal fentanyl exposure on sensory processing and function.


2021 ◽  
Vol 44 (1) ◽  
Author(s):  
Rainer W. Friedrich ◽  
Adrian A. Wanner

The dense reconstruction of neuronal wiring diagrams from volumetric electron microscopy data has the potential to generate fundamentally new insights into mechanisms of information processing and storage in neuronal circuits. Zebrafish provide unique opportunities for dynamical connectomics approaches that combine reconstructions of wiring diagrams with measurements of neuronal population activity and behavior. Such approaches have the power to reveal higher-order structure in wiring diagrams that cannot be detected by sparse sampling of connectivity and that is essential for neuronal computations. In the brain stem, recurrently connected neuronal modules were identified that can account for slow, low-dimensional dynamics in an integrator circuit. In the spinal cord, connectivity specifies functional differences between premotor interneurons. In the olfactory bulb, tuning-dependent connectivity implements a whitening transformation that is based on the selective suppression of responses to overrepresented stimulus features. These findings illustrate the potential of dynamical connectomics in zebrafish to analyze the circuit mechanisms underlying higher-order neuronal computations. Expected final online publication date for the Annual Review of Neuroscience, Volume 44 is July 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.


1997 ◽  
Vol 78 (1) ◽  
pp. 366-382 ◽  
Author(s):  
Earl L. Smith ◽  
Yuzo Chino ◽  
Jinren Ni ◽  
Han Cheng

Smith, Earl L., III, Yuzo Chino, Jinren Ni, and Han Cheng. Binocular combination of contrast signals by striate cortical neurons in the monkey. J. Neurophysiol. 78: 366–382, 1997. With the use of microelectrode recording techniques, we investigated how the contrast signals from the two eyes are combined in individual cortical neurons in the striate cortex of anesthetized and paralyzed macaque monkeys. For a given neuron, the optimal spatial frequency, orientation, and direction of drift for sine wave grating stimuli were determined for each eye. The cell's disparity tuning characteristics were determined by measuring responses as a function of the relative interocular spatial phase of dichoptic stimuli that consisted of the optimal monocular gratings. Binocular contrast summation was then investigated by measuring contrast response functions for optimal dichoptic grating pairs that had left- to right-eye interocular contrast ratios that varied from 0.1 to 10. The goal was to determine the left- and right-eye contrast components required to produce a criterion threshold response. For all functional classes of cortical neurons and for both cooperative and antagonistic binocular interactions, there was a linear relationship between the left- and right-eye contrast components required to produce a threshold response. Thus, for example for cooperative binocular interactions, a reduction in contrast to one eye was counterbalanced by an equivalent increase in contrast to the other eye. These results showed that in simple cells and phase-specific complex cells, the contrast signals from the two eyes were linearly combined at the subunit level before nonlinear rectification. In non-phase-specific complex cells, the linear binocular convergence of contrast signals could have taken place either before or after the rectification process, but before spike generation. In addition, for simple cells, vector analysis of spatial summation showed that the inputs from the two eyes were also combined in a linear manner before nonlinear spike-generating mechanisms. Thus simple cells showed linear spatial summation not only within and between subregions in a given receptive field, but also between the left- and right-eye receptive fields. Overall, the results show that the effectiveness of a stimulus in producing a response reflects interocular differences in the relative balance of inputs to a given cell, however, the eye of origin of a light-evoked signal has no specific consequence.


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.


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