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

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.

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.


2011 ◽  
Vol 106 (4) ◽  
pp. 1923-1932 ◽  
Author(s):  
Tomokazu Ohshiro ◽  
Shaista Hussain ◽  
Michael Weliky

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.


2016 ◽  
Vol 115 (5) ◽  
pp. 2556-2576 ◽  
Author(s):  
Vargha Talebi ◽  
Curtis L. Baker

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.


2014 ◽  
Vol 111 (11) ◽  
pp. 2355-2373 ◽  
Author(s):  
Stephen D. Van Hooser ◽  
Gina M. Escobar ◽  
Arianna Maffei ◽  
Paul Miller

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.


1984 ◽  
Vol 52 (5) ◽  
pp. 941-960 ◽  
Author(s):  
L. Tong ◽  
R. E. Kalil ◽  
P. D. Spear

Previous experiments have found that neurons in the cat's lateral suprasylvian (LS) visual area of cortex show functional compensation following removal of visual cortical areas 17, 18, and 19 on the day of birth. Correspondingly, an enhanced retino-thalamic pathway to LS cortex develops in these cats. The present experiments investigated the critical periods for these changes. Unilateral lesions of areas 17, 18, and 19 were made in cats ranging in age from 1 day postnatal to 26 wk. When the cats were adult, single-cell recordings were made from LS cortex ipsilateral to the lesion. In addition, transneuronal autoradiographic methods were used to trace the retino-thalamic projections to LS cortex in many of the same animals. Following lesions in 18- and 26-wk-old cats, there is a marked reduction in direction-selective LS cortex cells and an increase in cells that respond best to stationary flashing stimuli. These results are similar to those following visual cortex lesions in adult cats. In contrast, the percentages of cells with these properties are normal following lesions made from 1 day to 12 wk of age. Thus the critical period for development of direction selectivity and greater responses to moving than to stationary flashing stimuli in LS cortex following a visual cortex lesion ends between 12 and 18 wk of age. Following lesions in 26-wk-old cats, there is a decrease in the percentage of cells that respond to the ipsilateral eye, which is similar to results following visual cortex lesions in adult cats. However, ocular dominance is normal following lesions made from 1 day to 18 wk of age. Thus the critical period for development of responses to the ipsilateral eye following a lesion ends between 18 and 26 wk of age. Following visual cortex lesions in 2-, 4-, or 8-wk-old cats, about 30% of the LS cortex cells display orientation selectivity to elongated slits of light. In contrast, few or no cells display this property in normal adult cats, cats with lesions made on the day of birth, or cats with lesions made at 12 wk of age or later. Thus an anomalous property develops for many LS cells, and the critical period for this property begins later (between 1 day and 2 wk) and ends earlier (between 8 and 12 wk) than those for other properties.(ABSTRACT TRUNCATED AT 400 WORDS)


1976 ◽  
Vol 39 (3) ◽  
pp. 613-630 ◽  
Author(s):  
W. Singer ◽  
F. Tretter

An attempt was made to relate the alterations of cortical receptive fields as they result from binocular visual deprivation to changes in afferent, intrinsic, and efferent connections of the striate and parastriate cortex. The experiments were performed in cats aged at least 1 jr with their eyelids sutured closed from birth.The results of the receptive-field analysis in A17 confirmed the reduction of light-responsive cells, the occasional incongruity of receptive-field properties in the two eyes, and to some extent also the loss of orientation and direction selectivity as reported previously. Other properties common to numerous deprived receptive fields were the lack of sharp inhibitory sidebands and the sometimes exceedingly large size of the receptive fields. Qualitatively as well as quantitatively, similar alterations were observed in area 18. A rather high percentage of cells in both areas had, however, preserved at least some orientation preference, and a few receptive fields had tuning properties comparable to those in normal cats. The ability of area 18 cells in normal cats to respond to much higher stimulus velocities than area 17 cells was not influenced by deprivation.The results obtained with electrical stimulation suggest two main deprivation effects: 1) A marked decrease in the safety factor of retinothalamic and thalamocortical transmission. 2) A clear decrease in efficiency of intracortical inhibition. But the electrical stimulation data also show that none of the basic principles of afferent, intrinsic, and efferent connectivity is lost or changed by deprivation. The conduction velocities in the subcortical afferents and the differentiation of the afferents to areas 17 and 18 into slow- and fast-conducting projection systems remain unaltered. Intrinsic excitatory connections remain functional; this is also true for the disynaptic inhibitory pathways activated preferentially by the fast-conducting thalamocortical projection. The laminar distribution of cells with monosynaptic versus polsynaptic excitatory connections is similar to that in normal cats. Neurons with corticofugal axons remain functionally connected and show the same connectivity pattern as those in normal cats. The nonspecific activation system from the mesencephalic reticular formation also remains functioning both at the thalamic and the cortical level.We conclude from these and several other observations that most, if not all, afferent, intrinsic, and efferent connections of areas 17 and 18 are specified from birth and depend only little on visual experience. This predetermined structural plan, however, allows for some freedom in the domain of orientation tuning, binocular correspondence, and retinotopy which is specified only when visual experience is possible.


2020 ◽  
Author(s):  
Lukas Klimmasch ◽  
Johann Schneider ◽  
Alexander Lelais ◽  
Bertram E. Shi ◽  
Jochen Triesch

AbstractThe development of binocular vision is an active learning process comprising the development of disparity tuned neurons in visual cortex and the establishment of precise vergence control of the eyes. We present a computational model for the learning and self-calibration of active binocular vision based on the Active Efficient Coding framework, an extension of classic efficient coding ideas to active perception. Under normal rearing conditions, the model develops disparity tuned neurons and precise vergence control, allowing it to correctly interpret random dot stereogramms. Under altered rearing conditions modeled after neurophysiological experiments, the model qualitatively reproduces key experimental findings on changes in binocularity and disparity tuning. Furthermore, the model makes testable predictions regarding how altered rearing conditions impede the learning of precise vergence control. Finally, the model predicts a surprising new effect that impaired vergence control affects the statistics of orientation tuning in visual cortical neurons.


2019 ◽  
Author(s):  
Marie Tolkiehn ◽  
Simon R. Schultz

AbstractOrientation tuning in mouse primary visual cortex (V1) has long been reported to have a random or “salt-and-pepper” organisation, lacking the structure found in cats and primates. Laminar in-vivo multi-electrode array recordings here reveal previously elusive structure in the representation of visual patterns in the mouse visual cortex, with temporo-nasally drifting gratings eliciting consistently highest neuronal responses across cortical layers and columns, whilst upward moving gratings reliably evoked the lowest activities. We suggest this bias in direction selectivity to be behaviourally relevant as objects moving into the visual field from the side or behind may pose a predatory threat to the mouse whereas upward moving objects do not. We found furthermore that direction preference and selectivity was affected by stimulus spatial frequency, and that spatial and directional tuning curves showed high signal correlations decreasing with distance between recording sites. In addition, we show that despite this bias in direction selectivity, it is possible to decode stimulus identity and that spatiotemporal features achieve higher accuracy in the decoding task whereas spike count or population counts are sufficient to decode spatial frequencies implying different encoding strategies.Significance statementWe show that temporo-nasally drifting gratings (i.e. opposite the normal visual flow during forward movement) reliably elicit the highest neural activity in mouse primary visual cortex, whereas upward moving gratings reliably evoke the lowest responses. This encoding may be highly behaviourally relevant, as objects approaching from the periphery may pose a threat (e.g. predators), whereas upward moving objects do not. This is a result at odds with the belief that mouse primary visual cortex is randomly organised. Further to this biased representation, we show that direction tuning depends on the underlying spatial frequency and that tuning preference is spatially correlated both across layers and columns and decreases with cortical distance, providing evidence for structural organisation in mouse primary visual cortex.


2008 ◽  
Vol 100 (3) ◽  
pp. 1476-1487 ◽  
Author(s):  
Bin Zhang ◽  
Earl L. Smith ◽  
Yuzo M. Chino

Vision of newborn infants is limited by immaturities in their visual brain. In adult primates, the transient onset discharges of visual cortical neurons are thought to be intimately involved with capturing the rapid succession of brief images in visual scenes. Here we sought to determine the responsiveness and quality of transient responses in individual neurons of the primary visual cortex (V1) and visual area 2 (V2) of infant monkeys. We show that the transient component of neuronal firing to 640-ms stationary gratings was as robust and as reliable as in adults only 2 wk after birth, whereas the sustained component was more sluggish in infants than in adults. Thus the cortical circuitry supporting onset transient responses is functionally mature near birth, and our findings predict that neonates, known for their “impoverished vision,” are capable of initiating relatively mature fixating eye movements and of performing in detection of simple objects far better than traditionally thought.


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