scholarly journals Emerging feed-forward inhibition allows the robust formation of direction selectivity in the developing ferret visual cortex

2014 ◽  
Vol 111 (11) ◽  
pp. 2355-2373 ◽  
Author(s):  
Stephen D. Van Hooser ◽  
Gina M. Escobar ◽  
Arianna Maffei ◽  
Paul Miller
Keyword(s):  
Visual Cortex ◽  
Cortical Neurons ◽  
Initial Conditions ◽  
Receptive Fields ◽  
Long Term Potentiation ◽  
Direction Selectivity ◽  
Feed Forward ◽  
Synaptic Competition ◽  
Eye Opening ◽  
Feed Forward Inhibition

The computation of direction selectivity requires that a cell respond to joint spatial and temporal characteristics of the stimulus that cannot be separated into independent components. Direction selectivity in ferret visual cortex is not present at the time of eye opening but instead develops in the days and weeks following eye opening in a process that requires visual experience with moving stimuli. Classic Hebbian or spike timing-dependent modification of excitatory feed-forward synaptic inputs is unable to produce direction-selective cells from unselective or weakly directionally biased initial conditions because inputs eventually grow so strong that they can independently drive cortical neurons, violating the joint spatial-temporal activation requirement. Furthermore, without some form of synaptic competition, cells cannot develop direction selectivity in response to training with bidirectional stimulation, as cells in ferret visual cortex do. We show that imposing a maximum lateral geniculate nucleus (LGN)-to-cortex synaptic weight allows neurons to develop direction-selective responses that maintain the requirement for joint spatial and temporal activation. We demonstrate that a novel form of inhibitory plasticity, postsynaptic activity-dependent long-term potentiation of inhibition (POSD-LTPi), which operates in the developing cortex at the time of eye opening, can provide synaptic competition and enables robust development of direction-selective receptive fields with unidirectional or bidirectional stimulation. We propose a general model of the development of spatiotemporal receptive fields that consists of two phases: an experience-independent establishment of initial biases, followed by an experience-dependent amplification or modification of these biases via correlation-based plasticity of excitatory inputs that compete against gradually increasing feed-forward inhibition.

scholarly journals Categorically distinct types of receptive fields in early visual cortex

2016 ◽  
Vol 115 (5) ◽  
pp. 2556-2576 ◽  
Author(s):  
Vargha Talebi ◽  
Curtis L. Baker
Keyword(s):  
Visual Cortex ◽  
System Identification ◽  
Cortical Neurons ◽  
Temporal Dynamics ◽  
High Reliability ◽  
Receptive Fields ◽  
Direction Selectivity ◽  
Natural Image ◽  
Visual Responses ◽  
Neurophysiological Studies

In the visual cortex, distinct types of neurons have been identified based on cellular morphology, response to injected current, or expression of specific markers, but neurophysiological studies have revealed visual receptive field (RF) properties that appear to be on a continuum, with only two generally recognized classes: simple and complex. Most previous studies have characterized visual responses of neurons using stereotyped stimuli such as bars, gratings, or white noise and simple system identification approaches (e.g., reverse correlation). Here we estimate visual RF models of cortical neurons using visually rich natural image stimuli and regularized regression system identification methods and characterize their spatial tuning, temporal dynamics, spatiotemporal behavior, and spiking properties. We quantitatively demonstrate the existence of three functionally distinct categories of simple cells, distinguished by their degree of orientation selectivity (isotropic or oriented) and the nature of their output nonlinearity (expansive or compressive). In addition, these three types have differing average values of several other properties. Cells with nonoriented RFs tend to have smaller RFs, shorter response durations, no direction selectivity, and high reliability. Orientation-selective neurons with an expansive output nonlinearity have Gabor-like RFs, lower spontaneous activity and responsivity, and spiking responses with higher sparseness. Oriented RFs with a compressive nonlinearity are spatially nondescript and tend to show longer response latency. Our findings indicate multiple physiologically defined types of RFs beyond the simple/complex dichotomy, suggesting that cortical neurons may have more specialized functional roles rather than lying on a multidimensional continuum.

scholarly journals Impact of acute visual experience on development of LGN receptive fields in the ferret

2021 ◽  
Author(s):  
Andrea K Stacy ◽  
Nathan A Schneider ◽  
Noah K Gilman ◽  
Stephen D Van Hooser
Keyword(s):  
Visual Cortex ◽  
Cortical Neurons ◽  
Visual Experience ◽  
Receptive Fields ◽  
Direction Selectivity ◽  
In Vivo Electrophysiology ◽  
Primate Visual Cortex ◽  
Before And After ◽  
Visual Cortical

Selectivity for direction of motion is a key feature of primary visual cortical neurons. Visual experience is required for direction selectivity in carnivore and primate visual cortex, but the circuit mechanisms of its formation remain incompletely understood. Here we examined how developing lateral geniculate nucleus (LGN) neurons may contribute to cortical direction selectivity. Using in vivo electrophysiology techniques, we examined LGN receptive field properties of visually naive female ferrets before and after exposure to 6 hours of motion stimuli in order to assess the effect of acute visual experience on LGN cell development. We found that acute experience with motion stimuli did not significantly affect the weak orientation or direction selectivity of LGN neurons. In addition, we found that neither latency nor sustainedness or transience of LGN neurons significantly changed with acute experience. These results suggest that the direction selectivity that emerges in cortex after acute experience is computed in cortex and cannot be explained by changes in LGN cells.

scholarly journals Thalamocortical control of feed–forward inhibition in awake somatosensory ‘barrel’ cortex

2002 ◽  
Vol 357 (1428) ◽  
pp. 1717-1727 ◽  
Author(s):  
Harvey A . Swadlow
Keyword(s):  
Cortical Neurons ◽  
Barrel Cortex ◽  
Receptive Fields ◽  
Intracortical Inhibition ◽  
Inhibitory Interneurons ◽  
Feed Forward ◽  
Spiny Neurons ◽  
Optimal Feed ◽  
Cortical Receptive Fields ◽  
Feed Forward Inhibition

Intracortical inhibition plays a role in shaping sensory cortical receptive fields and is mediated by both feed–forward and feedback mechanisms. Feed–forward inhibition is the faster of the two processes, being generated by inhibitory interneurons driven by monosynaptic thalamocortical (TC) input. In principle, feed–forward inhibition can prevent targeted cortical neurons from ever reaching threshold when TC input is weak. To do so, however, inhibitory interneurons must respond to TC input at low thresholds and generate spikes very quickly. A powerful feed–forward inhibition would sharpen the tuning characteristics of targeted cortical neurons, and interneurons with sensitive and broadly tuned receptive fields could mediate this process. Suspected inhibitory interneurons (SINs) with precisely these properties are found in layer 4 of the somatosensory (S1) ‘barrel’ cortex of rodents and rabbits. These interneurons lack the directional selectivity seen in most cortical spiny neurons and in ventrobasal TC afferents, but are much more sensitive than cortical spiny neurons to low–amplitude whisker displacements. This paper is concerned with the activation of S1 SINs by TC impulses, and with the consequences of this activation. Multiple TC neurons and multiple S1 SINs were simultaneously studied in awake rabbits, and cross–correlation methods were used to examine functional connectivity. The results demonstrate a potent, temporally precise, dynamic and highly convergent/divergent functional input from ventrobasal TC neurons to SINs of the topographically aligned S1 barrel. Whereas the extensive pooling of convergent TC inputs onto SINs generates sensitive and broadly tuned inhibitory receptive fields, the potent TC divergence onto many SINs generates sharply synchronous activity among these elements. This TC feed–forward inhibitory network is well suited to provide a fast, potent, sensitive and broadly tuned inhibition of targeted spiny neurons that will suppress spike generation following all but the most optimal feed–forward excitatory inputs.

scholarly journals Spatial Distribution of Contextual Interactions in Primary Visual Cortex and in Visual Perception

2000 ◽  
Vol 84 (4) ◽  
pp. 2048-2062 ◽  
Author(s):  
Mitesh K. Kapadia ◽  
Gerald Westheimer ◽  
Charles D. Gilbert
Keyword(s):  
Spatial Distribution ◽  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Receptive Fields ◽  
Human Perception ◽  
Spatial Arrangement ◽  
Orthogonal Axis ◽  
V1 Neurons ◽  
Contextual Interactions

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.

scholarly journals Orientation Tuning, But Not Direction Selectivity, Is Invariant to Temporal Frequency in Primary Visual Cortex

2005 ◽  
Vol 94 (2) ◽  
pp. 1336-1345 ◽  
Author(s):  
Bartlett D. Moore ◽  
Henry J. Alitto ◽  
W. Martin Usrey
Keyword(s):  
Visual Cortex ◽  
Primary Visual Cortex ◽  
Visual Stimulus ◽  
Visual Processing ◽  
Cortical Neurons ◽  
Temporal Frequency ◽  
Direction Selectivity ◽  
Orientation Tuning ◽  
Orientation Contrast ◽  
Wide Range

The activity of neurons in primary visual cortex is influenced by the orientation, contrast, and temporal frequency of a visual stimulus. This raises the question of how these stimulus properties interact to shape neuronal responses. While past studies have shown that the bandwidth of orientation tuning is invariant to stimulus contrast, the influence of temporal frequency on orientation-tuning bandwidth is unknown. Here, we investigate the influence of temporal frequency on orientation tuning and direction selectivity in area 17 of ferret visual cortex. For both simple cells and complex cells, measures of orientation-tuning bandwidth (half-width at half-maximum response) are ∼20–25° across a wide range of temporal frequencies. Thus cortical neurons display temporal-frequency invariant orientation tuning. In contrast, direction selectivity is typically reduced, and occasionally reverses, at nonpreferred temporal frequencies. These results show that the mechanisms contributing to the generation of orientation tuning and direction selectivity are differentially affected by the temporal frequency of a visual stimulus and support the notion that stability of orientation tuning is an important aspect of visual processing.

Orientation Selectivity Is Reduced by Monocular Deprivation in Combination With PKA Inhibitors

2002 ◽  
Vol 88 (4) ◽  
pp. 1933-1940 ◽  
Author(s):  
Chris J. Beaver ◽  
Quentin S. Fischer ◽  
Qinghua Ji ◽  
Nigel W. Daw
Keyword(s):  
Visual Cortex ◽  
Protein Kinase ◽  
Critical Period ◽  
Ocular Dominance ◽  
Receptive Fields ◽  
Direction Selectivity ◽  
Orientation Selectivity ◽  
Monocular Deprivation ◽  
Ocular Dominance Plasticity ◽  
Kinase A

We have previously shown that the protein kinase A (PKA) inhibitor, 8-chloroadenosine-3′,5′–monophosphorothioate (Rp-8-Cl-cAMPS), abolishes ocular dominance plasticity in the cat visual cortex. Here we investigate the effect of this inhibitor on orientation selectivity. The inhibitor reduces orientation selectivity in monocularly deprived animals but not in normal animals. In other words, PKA inhibitors by themselves do not affect orientation selectivity, nor does monocular deprivation by itself, but monocular deprivation in combination with a PKA inhibitor does affect orientation selectivity. This result is found for the receptive fields in both deprived and nondeprived eyes. Although there is a tendency for the orientation selectivity in the nondeprived eye to be higher than the orientation selectivity in the deprived eye, the orientation selectivity in both eyes is considerably less than normal. The result is striking in animals at 4 wk of age. The effect of the monocular deprivation on orientation selectivity is reduced at 6 wk of age and absent at 9 wk of age, while the effect on ocular dominance shifts is less changed in agreement with previous results showing that the critical period for orientation/direction selectivity ends earlier than the critical period for ocular dominance. We conclude that closure of one eye in combination with inhibition of PKA reduces orientation selectivity during the period that orientation selectivity is still mutable and that the reduction in orientation selectivity is transferred to the nondeprived eye.

scholarly journals Classical-contextual interactions in V1 may rely on dendritic computations

2018 ◽  
Author(s):  
Lei Jin ◽  
Bardia F. Behabadi ◽  
Monica P. Jadi ◽  
Chaithanya A. Ramachandra ◽  
Bartlett W. Mel
Keyword(s):  
Visual Cortex ◽  
Cortical Neurons ◽  
Pyramidal Neurons ◽  
Contextual Information ◽  
Flexible Substrate ◽  
Receptive Fields ◽  
Boundary Detection ◽  
Synaptic Interactions ◽  
Horizontal Connections ◽  
Local Circuits

AbstractA signature feature of the neocortex is the dense network of horizontal connections (HCs) through which pyramidal neurons (PNs) exchange “contextual” information. In primary visual cortex (V1), HCs are thought to facilitate boundary detection, a crucial operation for object recognition, but how HCs modulate PN responses to boundary cues within their classical receptive fields (CRF) remains unknown. We began by “asking” natural images, through a structured data collection and ground truth labeling process, what function a V1 cell should use to compute boundary probability from aligned edge cues within and outside its CRF. The “answer” was an asymmetric 2-D sigmoidal function, whose nonlinear form provides the first normative account for the “multiplicative” center-flanker interactions previously reported in V1 neurons (Kapadia et al. 1995, 2000; Polat et al. 1998). Using a detailed compartmental model, we then show that this boundary-detecting classical-contextual interaction function can be computed with near perfect accuracy by NMDAR-dependent spatial synaptic interactions within PN dendrites – the site where classical and contextual inputs first converge in the cortex. In additional simulations, we show that local interneuron circuitry activated by HCs can powerfully leverage the nonlinear spatial computing capabilities of PN dendrites, providing the cortex with a highly flexible substrate for integration of classical and contextual information.Significance StatementIn addition to the driver inputs that establish their classical receptive fields, cortical pyramidal neurons (PN) receive a much larger number of “contextual” inputs from other PNs through a dense plexus of horizontal connections (HCs). However by what mechanisms, and for what behavioral purposes, HC’s modulate PN responses remains unclear. We pursued these questions in the context of object boundary detection in visual cortex, by combining an analysis of natural boundary statistics with detailed modeling PNs and local circuits. We found that nonlinear synaptic interactions in PN dendrites are ideally suited to solve the boundary detection problem. We propose that PN dendrites provide the core computing substrate through which cortical neurons modulate each other’s responses depending on context.

scholarly journals The physiological basis for the computation of direction selectivity in the Drosophila OFF pathway

2021 ◽  
Author(s):  
Giordano Ramos-Traslosheros ◽  
Marion Silies
Keyword(s):  
Receptive Field ◽  
Cortical Neurons ◽  
Receptive Fields ◽  
Direction Selectivity ◽  
Physiological Basis ◽  
Motion Computation ◽  
Biological Substrate ◽  
Field Organization ◽  
Receptive Field Organization ◽  
Neuronal Computation

In Drosophila, direction-selective neurons implement a mechanism of motion computation similar to cortical neurons, using contrast-opponent receptive fields with ON and OFF subunits. It is not clear how the presynaptic circuitry of direction-selective neurons in the OFF pathway supports this computation, because all major inputs are OFF-rectified neurons. Here, we reveal the biological substrate for motion computation in the OFF pathway. Three interneurons, Tm2, Tm9 and CT1, also provide information about ON stimuli to the OFF direction-selective neuron T5 across its receptive field, supporting a contrast-opponent receptive field organization. Consistent with its prominent role in motion detection, variability in Tm9 receptive field properties is passed on to T5, and calcium decrements in Tm9 in response to ON stimuli are maintained across behavioral states, while spatial tuning is sharpened by active behavior. Together, our work shows how a key neuronal computation is implemented by its constituent neuronal circuit elements to ensure direction selectivity.

scholarly journals Spontaneous retinal waves generate long-range horizontal connectivity in visual cortex

2020 ◽  
Author(s):  
Jinwoo Kim ◽  
Min Song ◽  
Se-Bum Paik
Keyword(s):  
Visual Cortex ◽  
Long Range ◽  
Primary Visual Cortex ◽  
Cortical Neurons ◽  
Activity Patterns ◽  
Developmental Model ◽  
List Type ◽  
Retinal Waves ◽  
Horizontal Connections ◽  
Eye Opening

AbstractIn the primary visual cortex (V1) of higher mammals, long-range horizontal connections (LHCs) are observed to develop, linking iso-orientation domains of cortical tuning. It is unknown how this feature-specific wiring of circuitry develops before eye opening. Here, we show that LHCs in V1 may originate from spatio-temporally structured feedforward activities generated from spontaneous retinal waves. Using model simulations based on the anatomy and observed activity patterns of the retina, we show that waves propagating in retinal mosaics can initialize the wiring of LHCs by co-activating neurons of similar tuning, whereas equivalent random activities cannot induce such organizations. Simulations showed that emerged LHCs can produce the patterned activities observed in V1, matching topography of the underlying orientation map. We also confirmed that the model can also reproduce orientation-specific microcircuits in salt-and-pepper organizations in rodents. Our results imply that early peripheral activities contribute significantly to cortical development of functional circuits.HighlightsDevelopmental model of long-range horizontal connections (LHCs) in V1 is simulatedSpontaneous retinal waves generate feature-specific wiring of LHCs in visual cortexEmerged LHCs induce orientation-matching patterns of spontaneous cortical activityRetinal waves induce orientation-specific microcircuits of visual cortex in rodentsSignificance statementLong-range horizontal connections (LHCs) in the primary visual cortex (V1) are observed to emerge before the onset of visual experience, selectively connecting iso-domains of orientation maps. However, it is unknown how such tuning-specific wirings develop before eye-opening. Here, we show that LHCs in V1 originate from the tuning-specific activation of cortical neurons by spontaneous retinal waves during early developmental stages. Our simulations of a visual cortex model show that feedforward activities from the retina initialize the spatial organization of activity patterns in V1, which induces visual feature-specific wirings of V1 neurons. Our model also explains the origin of cortical microcircuits observed in rodents, suggesting that the proposed developmental mechanism is applicable universally to circuits of various mammalian species.

scholarly journals Development of cortical orientation selectivity in the absence of visual experience with contour

2011 ◽  
Vol 106 (4) ◽  
pp. 1923-1932 ◽  
Author(s):  
Tomokazu Ohshiro ◽  
Shaista Hussain ◽  
Michael Weliky
Keyword(s):  
Cortical Neurons ◽  
Computational Models ◽  
Visual Experience ◽  
Receptive Fields ◽  
Orientation Selectivity ◽  
Experimental Result ◽  
Full Development ◽  
Visual Inputs ◽  
Eye Opening ◽  
Visual Cortical

Visual cortical neurons are selective for the orientation of lines, and the full development of this selectivity requires natural visual experience after eye opening. Here we examined whether this selectivity develops without seeing lines and contours. Juvenile ferrets were reared in a dark room and visually trained by being shown a movie of flickering, sparse spots. We found that despite the lack of contour visual experience, the cortical neurons of these ferrets developed strong orientation selectivity and exhibited simple-cell receptive fields. This finding suggests that overt contour visual experience is unnecessary for the maturation of orientation selectivity and is inconsistent with the computational models that crucially require the visual inputs of lines and contours for the development of orientation selectivity. We propose that a correlation-based model supplemented with a constraint on synaptic strength dynamics is able to account for our experimental result.

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