scholarly journals Spatially distributed computation in cortical circuits

2021 ◽  
Author(s):  
Sergei Gepshtein ◽  
Ambarish Pawar ◽  
Sunwoo Kwon ◽  
Sergey Savelev ◽  
Thomas D Albright

The traditional view of neural computation in the cerebral cortex holds that sensory neurons are specialized, i.e., selective for certain dimensions of sensory stimuli. This view was challenged by evidence of contextual interactions between stimulus dimensions in which a neuron's response to one dimension strongly depends on other dimensions. Here we use methods of mathematical modeling, psychophysics, and electrophysiology to address shortcomings of the traditional view. Using a model of a generic cortical circuit, we begin with the simple demonstration that cortical responses are always distributed among neurons, forming characteristic waveforms, which we call neural waves. When stimulated by patterned stimuli, circuit responses arise by interference of neural waves. Resulting patterns of interference depend on interaction between stimulus dimensions. Comparison of these modeled responses with responses of biological vision makes it clear that the framework of neural wave interference provides a useful alternative to the standard concept of neural computation.

2018 ◽  
Author(s):  
Petr Znamenskiy ◽  
Mean-Hwan Kim ◽  
Dylan R. Muir ◽  
Maria Florencia Iacaruso ◽  
Sonja B. Hofer ◽  
...  

In the cerebral cortex, the interaction of excitatory and inhibitory synaptic inputs shapes the responses of neurons to sensory stimuli, stabilizes network dynamics1 and improves the efficiency and robustness of the neural code2–4. Excitatory neurons receive inhibitory inputs that track excitation5–8. However, how this co-tuning of excitation and inhibition is achieved by cortical circuits is unclear, since inhibitory interneurons are thought to pool the inputs of nearby excitatory cells and provide them with non-specific inhibition proportional to the activity of the local network9–13. Here we show that although parvalbumin-expressing (PV) inhibitory cells in mouse primary visual cortex make connections with the majority of nearby pyramidal cells, the strength of their synaptic connections is structured according to the similarity of the cells’ responses. Individual PV cells strongly inhibit those pyramidal cells that provide them with strong excitation and share their visual selectivity. This fine-tuning of synaptic weights supports co-tuning of inhibitory and excitatory inputs onto individual pyramidal cells despite dense connectivity between inhibitory and excitatory neurons. Our results indicate that individual PV cells are preferentially integrated into subnetworks of inter-connected, co-tuned pyramidal cells, stabilising their recurrent dynamics. Conversely, weak but dense inhibitory connectivity between subnetworks is sufficient to support competition between them, de-correlating their output. We suggest that the history and structure of correlated firing adjusts the weights of both inhibitory and excitatory connections, supporting stable amplification and selective recruitment of cortical subnetworks.


1979 ◽  
Vol 57 (2) ◽  
pp. 174-184 ◽  
Author(s):  
Y. C. Wong ◽  
H. C. Kwan ◽  
J. T. Murphy

In monkeys performing a handle-repositioning task involving primarily wrist flexion–extension (F–E) movements after a torque perturbation was delivered to the handle, single units were recorded extracellularly in the contralateral precentral cortex. Precentral neurons were identified by passive somatosensory stimulation, and were classified into five somatotopically organized populations. Based on electromyographic recordings, it was observed that flexors and extensors about the wrist joint were specifically involved in the repositioning of the handle, while many other muscles which act at the wrist and other forelimb joints were involved in the task in a supportive role. In precentral cortex, all neuronal responses observed were temporally correlated to both the sensory stimuli and the motor responses. Visual stimuli, presented simultaneously with torque perturbations, did not affect the early portion of cortical responses to such torque perturbations. In each of the five somatotopically organized neuronal populations, task-related neurons as well as task-unrelated ones were observed. A significantly larger proportion of wrist (F–E) neurons was related to the task, as compared with the other, nonwrist (F–E) populations. The above findings were discussed in the context of a hypothesis for the function of precentral cortex during voluntary limb movement in awake primates. This hypothesis incorporates a relationship between activities of populations of precentral neurons, defined with respect to their responses to peripheral events at or about single joints, and movements about the same joint.


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.


2006 ◽  
Vol 101 (2) ◽  
pp. 413-419 ◽  
Author(s):  
M. Waldmann ◽  
G. W. Thompson ◽  
G. C. Kember ◽  
J. L. Ardell ◽  
J. A. Armour

To quantify the concurrent transduction capabilities of spatially distributed intrinsic cardiac neurons, the activities generated by atrial vs. ventricular intrinsic cardiac neurons were recorded simultaneously in 12 anesthetized dogs at baseline and during alterations in the cardiac milieu. Few (3%) identified atrial and ventricular neurons (2 of 72 characterized neurons) responded solely to regional mechanical deformation, doing so in a tightly coupled fashion (cross-correlation coefficient r = 0.63). The remaining (97%) atrial and ventricular neurons transduced multimodal stimuli to display stochastic behavior. Specifically, ventricular chemosensory inputs modified these populations such that they generated no short-term coherence among their activities (cross-correlation coefficient r = 0.21 ± 0.07). Regional ventricular ischemia activated most atrial and ventricular neurons in a noncoupled fashion. Nicotinic activation of atrial neurons enhanced ventricular neuronal activity. Acute decentralization of the intrinsic cardiac nervous system obtunded its neuron responsiveness to cardiac sensory stimuli. Most atrial and ventricular intrinsic cardiac neurons generate concurrent stochastic activity that is predicated primarily upon their cardiac chemotransduction. As a consequence, they display relative independent short-term (beat-to-beat) control over regional cardiac indexes. Over longer time scales, their functional interdependence is manifest as the result of interganglionic interconnections and descending inputs.


eLife ◽  
2017 ◽  
Vol 6 ◽  
Author(s):  
Luis Carlos Garcia del Molino ◽  
Guangyu Robert Yang ◽  
Jorge F Mejias ◽  
Xiao-Jing Wang

Pyramidal cells and interneurons expressing parvalbumin (PV), somatostatin (SST), and vasoactive intestinal peptide (VIP) show cell-type-specific connectivity patterns leading to a canonical microcircuit across cortex. Experiments recording from this circuit often report counterintuitive and seemingly contradictory findings. For example, the response of SST cells in mouse V1 to top-down behavioral modulation can change its sign when the visual input changes, a phenomenon that we call response reversal. We developed a theoretical framework to explain these seemingly contradictory effects as emerging phenomena in circuits with two key features: interactions between multiple neural populations and a nonlinear neuronal input-output relationship. Furthermore, we built a cortical circuit model which reproduces counterintuitive dynamics observed in mouse V1. Our analytical calculations pinpoint connection properties critical to response reversal, and predict additional novel types of complex dynamics that could be tested in future experiments.


2007 ◽  
Vol 97 (4) ◽  
pp. 2992-3003 ◽  
Author(s):  
Aren J. Borgdorff ◽  
James F. A. Poulet ◽  
Carl C. H. Petersen

The sensory responses in the barrel cortex of mice aged postnatal day (P)7–P12 evoked by a single whisker deflection are smaller in amplitude and spread over a smaller area than those measured in P13–P21 mice. However, repetitive 10-Hz stimulation or paired pulse whisker stimulation in P7–P12 mice evoked facilitating sensory responses, contrasting with the depressing sensory responses observed in P13–P21 mice. This facilitation occurred during an interval ranging 300–1,000 ms after the first stimulus and was measured using whole cell recordings, voltage-sensitive dye imaging, and calcium-sensitive dye imaging. The facilitated responses were not only larger in amplitude but also propagated over a larger cortical area. The facilitation could be blocked by local application of pharmacological agents reducing cortical excitability. Local cortical microstimulation could substitute for the first whisker stimulus to produce a facilitated sensory response. The enhanced sensory responses evoked by repetitive sensory stimuli in P7–P12 mice may contribute to the activity-dependent specification of the developing cortical circuits. In addition, the facilitating sensory responses allow long integration times for sensory processing compatible with the slow behavior of mice during early postnatal development.


2021 ◽  
Author(s):  
Joseph T Francis ◽  
Anna Rozenboym ◽  
Lee von Kraus ◽  
Shaohua Xu ◽  
Pratik Chhatbar ◽  
...  

Lost sensations, such as touch, could be restored by microstimulation (MiSt) along the sensory neural substrate. Such neuroprosthetic sensory information can be used as feedback from an invasive brain-machine interface (BMI) to control a robotic arm/hand, such that tactile and proprioceptive feedback from the sensorized robotic arm/hand is directly given to the BMI user. Microstimulation in the human somatosensory thalamus (Vc) has been shown to produce somatosensory perceptions. However, until recently, systematic methods for using thalamic stimulation to evoke naturalistic touch perceptions were lacking. We have recently presented rigorous methods for determining a mapping between ventral posterior lateral thalamus (VPL) MiSt, and neural responses in the somatosensory cortex (S1), in a rodent model (Choi et al., 2016; Choi and Francis, 2018). Our technique minimizes the difference between S1 neural responses induced by natural sensory stimuli and those generated via VPL MiSt. Our goal is to develop systems that know what MiSt will produce a given neural response and possibly a more natural "sensation." To date, our optimization has been conducted in the rodent model and simulations. Here we present data from simple non-optimized thalamic MiSt during peri-operative experiments, where we MiSt in the VPL of macaques with a somatosensory system more like humans. We implanted arrays of microelectrodes across the hand area of the macaque S1 cortex as well as in the VPL thalamus. Multi and single-unit recordings were used to compare cortical responses to natural touch and thalamic MiSt in the anesthetized state. Post stimulus time histograms were highly correlated between the VPL MiSt and natural touch modalities, adding support to the use of VPL MiSt towards producing a somatosensory neuroprosthesis in humans.


Author(s):  
Katarzyna Kordecka ◽  
Andrzej T. Foik ◽  
Agnieszka Wierzbicka ◽  
Wioletta J. Waleszczyk

AbstractRepetitive visual stimulation is successfully used in a study on the visual evoked potential (VEP) plasticity in the visual system in mammals. Practicing visual tasks or repeated exposure to sensory stimuli can induce neuronal network changes in the cortical circuits and improve the perception of these stimuli. However little is known about the effect of visual training at the subcortical level. In the present study, we extend the knowledge showing positive results of this training in the rat’s superior colliculus (SC). In electrophysiological experiments, we showed that a single training session lasting several hours induces a response enhancement both in the primary visual cortex (V1) and in the SC. Further, we tested if collicular responses will be enhanced without V1 input. For this reason, we inactivated the V1 by applying xylocaine solution onto the cortical surface during visual training. Our results revealed that SC’s response enhancement was present even without V1 inputs and showed no difference in amplitude comparing to VEPs enhancement while the V1 was active. These data suggest that the visual system plasticity and facilitation can develop independently but simultaneously in different parts of the visual system.


2018 ◽  
Author(s):  
Jackson J. Cone ◽  
Megan D. Scantlen ◽  
Mark H. Histed ◽  
John H.R. Maunsell

SummaryWhile recent work has revealed how different inhibitory interneurons influence cortical responses to sensory stimuli, little is known about how their activity contributes to sensory perception. Here, we optogenetically stimulated different genetically defined interneurons (parvalbumin (PV), somatostatin (SST), vasoactive intestinal peptide (VIP)) in visual cortex (V1) of mice working at threshold in contrast increment or decrement detection tasks. The visual stimulus was paired with optogenetic stimulation to assess how enhancing V1 inhibitory neuron activity synchronously during cortical responses altered task performance. PV or SST activation impaired, while VIP stimulation improved, contrast increment detection. Notably, PV or SST stimulation also impaired contrast decrement detection, when opsin-evoked inhibition would exaggerate stimulus-evoked decrements in firing rate, and thus might improve performance. The impairment produced by PV or SST stimulation persisted throughout many weeks of testing. In contrast mice learned to reliably detect VIP activation in the absence of natural visual stimulation. Thus, different inhibitory signals make distinct contributions to visual contrast perception.


2018 ◽  
Author(s):  
Jordan P. Hamm ◽  
Yuriy Shymkiv ◽  
Shuting Han ◽  
Weijian Yang ◽  
Rafael Yuste

AbstractCortical processing of sensory events is significantly influenced by context. For instance, a repetitive or redundant visual stimulus elicits attenuated cortical responses, but if the same stimulus is unexpected or “deviant”, responses are augmented. This contextual modulation of sensory processing is likely a fundamental function of neural circuits, yet an understanding of how it is computed is still missing. Using holographic two-photon calcium imaging in awake animals, here we identify three distinct, spatially intermixed ensembles of neurons in mouse primary visual cortex which differentially respond to the same stimulus under separate contexts, including a subnetwork which selectively responds to deviant events. These non-overlapping ensembles are distributed across layers 2-5, though deviance detection is more common in superficial layers. Contextual preferences likely arise locally since they are not present in bottom up inputs from the thalamus or top-down inputs from prefrontal cortex. The functional parcellation of cortical circuits into independent ensembles that encode stimulus context provides a circuit basis underlying cortically based perception of novel or redundant stimuli, a key deficit in many psychiatric disorders.One Sentence SummaryVisual cortex represents deviant and redundant stimuli with separate subnetworks.


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