Learning enhances encoding of time and temporal surprise in primary sensory cortex

Primary sensory cortex has long been believed to play a straightforward role in the initial processing of sensory information. Yet, the superficial layers of cortex overall are sparsely active, even during sensory stimulation; moreover, cortical activity is influenced by other modalities, task context, reward, and behavioral state. Our study demonstrates that reinforcement learning dramatically alters representations among longitudinally imaged neurons in superficial layers of mouse primary somatosensory cortex. Learning an object detection task recruits previously unresponsive neurons, enlarging the neuronal population sensitive to touch and behavioral choice. In contrast, cortical responses decrease upon repeated exposure to unrewarded stimuli. Moreover, training improved population encoding of the passage of time, and unexpected deviations in trial timing elicited even stronger responses than touch did. In conclusion, the superficial layers of sensory cortex exhibit a high degree of learning-dependent plasticity and are strongly modulated by non-sensory but behaviorally-relevant features, such as timing and surprise.

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Role of Primary Sensory Cortex in Generalized Electrocortical Activation

American Journal of Physiology-Legacy Content ◽

10.1152/ajplegacy.1957.189.1.137 ◽

1957 ◽

Vol 189 (1) ◽

pp. 137-140

Author(s):

Aaron J. Beller ◽

Gidon F. Gestring ◽

Dominick P. Purpura

Keyword(s):

Sensory Stimulation ◽

Sensory Cortex ◽

Activation Process ◽

Afferent Activity ◽

Primary Sensory Cortex ◽

Cortical Regions ◽

Somatic Sensory Cortex ◽

Bilateral Destruction

Experiments were performed on intact unanesthetized-succinylcholine paralyzed cats in order to compare the effects of ablations of primary cortical regions on the ability to evoke generalized activation to specific sensory stimulation with those obtained by Bremer on encéphale isolé preparations. Bilateral destruction of the auditory or somatic sensory cortex in intact preparations does not block generalized activation to auditory or sciatic stimulation. It is concluded that in the presence of spinal afferent activity as exists in the intact preparation corticifugal influences arising in either the auditory or somatic sensory cortex are not necessary for the activation process that follows auditory or sciatic stimulation.

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Thalamocortical spectral transmission relies on balanced input strengths

10.1101/2020.09.20.305136 ◽

2020 ◽

Author(s):

Matteo Saponati ◽

Jordi Garcia-Ojalvo ◽

Enrico Cataldo ◽

Alberto Mazzoni

Keyword(s):

Sensory Information ◽

Field Potential ◽

Sensory Cortex ◽

Inhibitory Neurons ◽

Spectral Transmission ◽

Sensory Transmission ◽

Thalamocortical Connections ◽

Primary Sensory Cortex ◽

Spiking Network ◽

The Brain

AbstractThe thalamus is a key element of sensory transmission in the brain, as all sensory information is processed by the thalamus before reaching the cortex. The thalamus is known to gate and select sensory streams through a modulation of its internal activity in which spindle oscillations play a preponderant role, but the mechanism underlying this process is not completely understood. In particular, how do thalamocortical connections convey stimulus-driven information selectively over the background of thalamic internally generated activity (such as spindle oscillations)? Here we investigate this issue with a spiking network model of connectivity between thalamus and primary sensory cortex reproducing the local field potential of both areas. We found two features of the thalamocortical dynamics that filter out spindle oscillations: i) spindle oscillations are weaker in neurons projecting to the cortex, ii) the resonance dynamics of cortical networks selectively blocks frequency in the range encompassing spindle oscillations. This latter mechanism depends on the balance of the strength of thalamocortical connections toward excitatory and inhibitory neurons in the cortex. Our results pave the way toward an integrated understanding of the sensory streams traveling between the periphery and the cortex.

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Cortical ensembles selective for context

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.2026179118 ◽

2021 ◽

Vol 118 (14) ◽

pp. e2026179118

Author(s):

Jordan P. Hamm ◽

Yuriy Shymkiv ◽

Shuting Han ◽

Weijian Yang ◽

Rafael Yuste

Keyword(s):

Sensory Information ◽

Prediction Errors ◽

Cortical Circuits ◽

Two Photon ◽

Specific Subset ◽

Primary Sensory Cortex ◽

Cortical Responses ◽

And Behavior ◽

Visual Oddball ◽

Selection Of

Neural processing of sensory information is strongly influenced by context. For instance, cortical responses are reduced to predictable stimuli, while responses are increased to novel stimuli that deviate from contextual regularities. Such bidirectional modulation based on preceding sensory context is likely a critical component or manifestation of attention, learning, and behavior, yet how it arises in cortical circuits remains unclear. Using volumetric two-photon calcium imaging and local field potentials in primary visual cortex (V1) from awake mice presented with visual “oddball” paradigms, we identify both reductions and augmentations of stimulus-evoked responses depending, on whether the stimulus was redundant or deviant, respectively. Interestingly, deviance-augmented responses were limited to a specific subset of neurons mostly in supragranular layers. These deviance-detecting cells were spatially intermixed with other visually responsive neurons and were functionally correlated, forming a neuronal ensemble. Optogenetic suppression of prefrontal inputs to V1 reduced the contextual selectivity of deviance-detecting ensembles, demonstrating a causal role for top-down inputs. The presence of specialized context-selective ensembles in primary sensory cortex, modulated by higher cortical areas, provides a circuit substrate for the brain’s construction and selection of prediction errors, computations which are key for survival and deficient in many psychiatric disorders.

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Short term plasticity of the primary sensory cortex revealed by interventions contralateral to the stimulus in Median nerve SEP

Klinische Neurophysiologie ◽

10.1055/s-2006-939314 ◽

2006 ◽

Vol 37 (01) ◽

Author(s):

T Waberski ◽

A Dieckhöfer ◽

U Reminghorst ◽

H Buchner ◽

R Gobbelé

Keyword(s):

Median Nerve ◽

Sensory Cortex ◽

Short Term ◽

Short Term Plasticity ◽

Primary Sensory Cortex

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Sensory over-responsivity is related to GABAergic inhibition in thalamocortical circuits

Translational Psychiatry ◽

10.1038/s41398-020-01154-0 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Emily T. Wood ◽

Kaitlin K. Cummings ◽

Jiwon Jung ◽

Genevieve Patterson ◽

Nana Okada ◽

...

Keyword(s):

Magnetic Resonance ◽

Sensory Information ◽

Network Connectivity ◽

Sensory Stimulation ◽

Autism Spectrum ◽

Future Research ◽

Resonance Spectroscopy ◽

Gamma Aminobutyric Acid ◽

Sensory Stimuli ◽

Brain Responses

AbstractSensory over-responsivity (SOR), extreme sensitivity to or avoidance of sensory stimuli (e.g., scratchy fabrics, loud sounds), is a highly prevalent and impairing feature of neurodevelopmental disorders such as autism spectrum disorders (ASD), anxiety, and ADHD. Previous studies have found overactive brain responses and reduced modulation of thalamocortical connectivity in response to mildly aversive sensory stimulation in ASD. These findings suggest altered thalamic sensory gating which could be associated with an excitatory/inhibitory neurochemical imbalance, but such thalamic neurochemistry has never been examined in relation to SOR. Here we utilized magnetic resonance spectroscopy and resting-state functional magnetic resonance imaging to examine the relationship between thalamic and somatosensory cortex inhibitory (gamma-aminobutyric acid, GABA) and excitatory (glutamate) neurochemicals with the intrinsic functional connectivity of those regions in 35 ASD and 35 typically developing pediatric subjects. Although there were no diagnostic group differences in neurochemical concentrations in either region, within the ASD group, SOR severity correlated negatively with thalamic GABA (r = −0.48, p < 0.05) and positively with somatosensory glutamate (r = 0.68, p < 0.01). Further, in the ASD group, thalamic GABA concentration predicted altered connectivity with regions previously implicated in SOR. These variations in GABA and associated network connectivity in the ASD group highlight the potential role of GABA as a mechanism underlying individual differences in SOR, a major source of phenotypic heterogeneity in ASD. In ASD, abnormalities of the thalamic neurochemical balance could interfere with the thalamic role in integrating, relaying, and inhibiting attention to sensory information. These results have implications for future research and GABA-modulating pharmacologic interventions.

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Linking sensory neurons to visually guided behavior: Relating MST activity to steering in a virtual environment

Visual Neuroscience ◽

10.1017/s0952523813000412 ◽

2013 ◽

Vol 30 (5-6) ◽

pp. 315-330 ◽

Cited By ~ 2

Author(s):

SETH W. EGGER ◽

KENNETH H. BRITTEN

Keyword(s):

Cortical Neurons ◽

Traditional Approach ◽

Sensory System ◽

Sensory Information ◽

Neuronal Population ◽

Difficult Problem ◽

Lower Envelope ◽

Visually Guided ◽

Medial Superior Temporal ◽

Visual Cortical

AbstractMany complex behaviors rely on guidance from sensations. To perform these behaviors, the motor system must decode information relevant to the task from the sensory system. However, identifying the neurons responsible for encoding the appropriate sensory information remains a difficult problem for neurophysiologists. A key step toward identifying candidate systems is finding neurons or groups of neurons capable of representing the stimuli adequately to support behavior. A traditional approach involves quantitatively measuring the performance of single neurons and comparing this to the performance of the animal. One of the strongest pieces of evidence in support of a neuronal population being involved in a behavioral task comes from the signals being sufficient to support behavior. Numerous experiments using perceptual decision tasks show that visual cortical neurons in many areas have this property. However, most visually guided behaviors are not categorical but continuous and dynamic. In this article, we review the concept of sufficiency and the tools used to measure neural and behavioral performance. We show how concepts from information theory can be used to measure the ongoing performance of both neurons and animal behavior. Finally, we apply these tools to dorsal medial superior temporal (MSTd) neurons and demonstrate that these neurons can represent stimuli important to navigation to a distant goal. We find that MSTd neurons represent ongoing steering error in a virtual-reality steering task. Although most individual neurons were insufficient to support the behavior, some very nearly matched the animal’s estimation performance. These results are consistent with many results from perceptual experiments and in line with the predictions of Mountcastle’s “lower envelope principle.”

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Optimization of sensory stimulation for neuronal population activity

BMC Neuroscience ◽

10.1186/1471-2202-11-s1-p178 ◽

2010 ◽

Vol 11 (S1) ◽

Author(s):

Noelia Montejo ◽

Jean-Luc Blanc ◽

Yann Mahnoun ◽

Jean-Michel Brezun ◽

Nicolas Catz ◽

...

Keyword(s):

Sensory Stimulation ◽

Neuronal Population ◽

Population Activity

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Inter- and intra-hemispheric spatiotemporal organization of spontaneous electrocortical oscillations

Journal of Neurophysiology ◽

10.1152/jn.1996.76.1.423 ◽

1996 ◽

Vol 76 (1) ◽

pp. 423-437 ◽

Cited By ~ 18

Author(s):

K. D. MacDonald ◽

B. Brett ◽

D. S. Barth

Keyword(s):

Time Series ◽

Somatosensory Cortex ◽

Phase Locking ◽

Sensory Information ◽

Gamma Oscillations ◽

Sensory Cortex ◽

Electrode Arrays ◽

Sharp Wave ◽

Lower Amplitude ◽

The Right

1. Two 64-channel epipial electrode arrays were positioned on homologous locations of the right and left hemisphere, covering most of primary and secondary auditory and somatosensory cortex in eight lightly anesthetized rats. Array placement was verified with the use of cytochrome oxidase histochemistry. 2. Middle-latency auditory and somatosensory evoked potentials (MAEPs and MSEPs, respectively) and spontaneous oscillations in the frequency range of 20-40 Hz (gamma oscillations) were recorded and found to be spatially constrained to regions of granular cortex, suggesting that both phenomena are closely associated with sensory information processing. 3. The MAEP and MSEP consisted of an initial biphasic sharp wave in primary auditory and somatosensory cortex, respectively, and a similar biphasic sharp wave occurred approximately 4-8 ms later in secondary sensory cortex of the given modality. Averaged gamma oscillations also revealed asynchronous activation of sensory cortex, but with a shorter 2-ms delay between oscillations in primary and secondary regions. Although the long latency shift of the MAEP and MSEP may be due in part to asynchronous activation of parallel thalamocortical projections to primary and secondary sensory cortex, the much shorter shift of gamma oscillations in a given modality is consistent with intracortical coupling of these regions. 4. Gamma oscillations occurred independently in auditory and somatosensory cortex within a given hemisphere. Furthermore, time series averaging revealed that there was no phase-locking of oscillations between the sensory modalities. 5. Gamma oscillations were loosely coupled between hemispheres; oscillations occurring in auditory or somatosensory cortex of one hemisphere were often associated with lower-amplitude oscillations in homologous contralateral sensory cortex. Yet, the fact that time series averaging revealed no interhemispheric phase-locking suggests that the corpus callosum may not coordinate the bilateral gamma oscillations, and that a thalamic modulatory influence may be involved.

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New Models for Motor Control

Neural Computation ◽

10.1162/neco.1989.1.2.173 ◽

1989 ◽

Vol 1 (2) ◽

pp. 173-183 ◽

Cited By ~ 28

Author(s):

Jennifer S. Altman ◽

Jenny Kien

Keyword(s):

Distributed Control ◽

Hierarchical Control ◽

Sensory Information ◽

Striking Similarity ◽

Maximum Efficiency ◽

Behavioral Choice ◽

Modular Control ◽

Superficial Resemblance ◽

Different Levels ◽

Command Center

What do a prototype robot (Brooks 1989) and a model for the control of behavioral choice in insects (Altman and Kien 1987a) have in common? And what do they share with a scratching cat (Shadmehr 1989)? The answer is distributed control systems that do not depend on a central command center for the execution of behavioral outputs. The first two in particular are examples of a growing trend to replace the long-held concept of linear hierarchical control of motor output with one of decentralized, distributed control, with inputs at many levels and the output a consensus of the activity in several centers. Brooks (1989) describes a six-legged machine that, in its most advanced form, can walk over rough terrain and prowl around following a source of warmth, such as a person. The six legs, chosen as a compromise between stability and ease of coordination, give the robot a superficial resemblance to an insect — but the similarity goes deeper. The modular control system, designed strictly on engineering principles for maximum efficiency and economy, bears a striking similarity to the model we have proposed elsewhere (Altman and Kien 1987a) to describe the organization of the motor system in insects such as the locust. In both systems, the same set of components can generate different behaviors, depending on the context, and similar principles govern the generation of different levels of behavior, from movements of a single leg to coordinated responses of the whole beast. Neither requires a single center for integrating all sensory information and conflicts tend to be resolved by consensus at the motor level.

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