scholarly journals Synaptic and intrinsic mechanisms underlying development of cortical direction selectivity

2019 ◽  
Author(s):  
Arani Roy ◽  
Jason J. Osik ◽  
Benyamin Meschede-Krasa ◽  
Wesley Alford ◽  
Daniel P. Leman ◽  
...  

AbstractSome neural circuits are constructed through an overproduction of initial connections followed by activity-dependent refinement. Under this paradigm, functional receptive fields would be expected to be narrowed from a diffuse immature condition to a sharper mature condition. Alternatively, neural activity might lead to formation of new connections, leading to expansion of an initially compact receptive field. In the simple cells of the ferret visual cortex undergoing developmental enhancement of direction selectivity, we found evidence for a mixed mechanism: an expansion of the spatiotemporal receptive fields along the temporal dimension combined with a narrowing in space-time through a marked loss of inputs with certain space-time selectivities. Further, the resulting increase in subthreshold direction selectivity was accompanied by increases in near-spike-threshold excitability and input-output gain that resulted in dramatically increased spiking responses. Increases in subthreshold membrane responses and the increased input-output spiking gain were both necessary to explain firing rates in experienced ferrets. These results demonstrate that cortical direction selectivity develops through a combination of plasticity in synaptic and cell-intrinsic properties.

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Arani Roy ◽  
Jason J Osik ◽  
Benyamin Meschede-Krasa ◽  
Wesley T Alford ◽  
Daniel P Leman ◽  
...  

Modifications of synaptic inputs and cell-intrinsic properties both contribute to neuronal plasticity and development. To better understand these mechanisms, we undertook an intracellular analysis of the development of direction selectivity in the ferret visual cortex, which occurs rapidly over a few days after eye opening. We found strong evidence of developmental changes in linear spatiotemporal receptive fields of simple cells, implying alterations in circuit inputs. Further, this receptive field plasticity was accompanied by increases in near-spike-threshold excitability and input-output gain that resulted in dramatically increased spiking responses in the experienced state. Increases in subthreshold membrane responses induced by the receptive field plasticity and the increased input-output spiking gain were both necessary to explain the elevated firing rates in experienced ferrets. These results demonstrate that cortical direction selectivity develops through a combination of plasticity in inputs and in cell-intrinsic properties.


2015 ◽  
Vol 114 (1) ◽  
pp. 540-550 ◽  
Author(s):  
James T. Pearson ◽  
Daniel Kerschensteiner

Contrast, a fundamental feature of visual scenes, is encoded in a distributed manner by ∼20 retinal ganglion cell (RGC) types, which stream visual information to the brain. RGC types respond preferentially to positive (ONpref) or negative (OFFpref) contrast and differ in their sensitivity to preferred contrast and responsiveness to nonpreferred stimuli. Vision operates over an enormous range of mean light levels. The influence of ambient illumination on contrast encoding across RGC types is not well understood. Here, we used large-scale multielectrode array recordings to characterize responses of mouse RGCs under lighting conditions spanning five orders in brightness magnitude. We identify three functional RGC types that switch contrast preference in a luminance-dependent manner (Sw1-, Sw2-, and Sw3-RGCs). As ambient illumination increases, Sw1- and Sw2-RGCs shift from ONpref to OFFpref and Sw3-RGCs from OFFpref to ONpref. In all cases, transitions in contrast preference are reversible and track light levels. By mapping spatiotemporal receptive fields at different mean light levels, we find that changes in input from ON and OFF pathways in receptive field centers underlie shifts in contrast preference. Sw2-RGCs exhibit direction-selective responses to motion stimuli. Despite changing contrast preference, direction selectivity of Sw2-RGCs and other RGCs as well as orientation-selective responses of RGCs remain stable across light levels.


1999 ◽  
Vol 11 (5) ◽  
pp. 1079-1096 ◽  
Author(s):  
Jorge Golowasch ◽  
Michael Casey ◽  
L. F. Abbott ◽  
Eve Marder

Activity-dependent plasticity appears to play an important role in the modification of neurons and neural circuits that occurs during development and learning. Plasticity is also essential for the maintenance of stable patterns of activity in the face of variable environmental and internal conditions. Previous theoretical and experimental results suggest that neurons stabilize their activity by altering the number or characteristics of ion channels to regulate their intrinsic electrical properties. We present both experimental and modeling evidence to show that activity-dependent regulation of conductances, operating at the level of individual neurons, can also stabilize network activity. These results indicate that the stomatogastric ganglion of the crab can generate a characteristic rhythmic pattern of activity in two fundamentally different modes of operation. In one mode, the rhythm is strictly conditional on the presence of neuromodulatory afferents from adjacent ganglia. In the other, it is independent of neuromodulatory input but relies on newly developed intrinsic properties of the component neurons.


1993 ◽  
Vol 90 (23) ◽  
pp. 11142-11146 ◽  
Author(s):  
S Bisti ◽  
C Trimarchi

Prenatal unilateral enucleation in mammals causes an extensive anatomical reorganization of visual pathways. The remaining eye innervates the entire extent of visual subcortical and cortical areas. Electrophysiological recordings have shown that the retino-geniculate connections are retinotopically organized and geniculate neurones have normal receptive field properties. In area 17 all neurons respond to stimulation of the remaining eye and retinotopy, orientation columns, and direction selectivity are maintained. The only detectable change is a reduction in receptive field size. Are these changes reflected in the visual behavior? We studied visual performance in cats unilaterally enucleated 3 weeks before birth (gestational age at enucleation, 39-42 days). We tested behaviorally the development of visual acuity and, in the adult, the extension of the visual field and the contrast sensitivity. We found no difference between prenatal monocularly enucleated cats and controls in their ability to orient to targets in different positions of the visual field or in their visual acuity (at any age). The major difference between enucleated and control animals was in contrast sensitivity:prenatal enucleated cats present a loss in sensitivity for gratings of low spatial frequency (below 0.5 cycle per degree) as well as a slight increase in sensitivity at middle frequencies. We conclude that prenatal unilateral enucleation causes a selective change in the spatial performance of the remaining eye. We suggest that this change is the result of a reduction in the number of neurones with large receptive fields, possibly due to a severe impairment of the Y system.


2005 ◽  
Vol 94 (6) ◽  
pp. 4156-4167 ◽  
Author(s):  
Daniel Zaksas ◽  
Tatiana Pasternak

Neurons in cortical area MT have localized receptive fields (RF) representing the contralateral hemifield and play an important role in processing visual motion. We recorded the activity of these neurons during a behavioral task in which two monkeys were required to discriminate and remember visual motion presented in the ipsilateral hemifield. During the task, the monkeys viewed two stimuli, sample and test, separated by a brief delay and reported whether they contained motion in the same or in opposite directions. Fifty to 70% of MT neurons were activated by the motion stimuli presented in the ipsilateral hemifield at locations far removed from their classical receptive fields. These responses were in the form of excitation or suppression and were delayed relative to conventional MT responses. Both excitatory and suppressive responses were direction selective, but the nature and the time course of their directionality differed from the conventional excitatory responses recorded with stimuli in the RF. Direction selectivity of the excitatory remote response was transient and early, whereas the suppressive response developed later and persisted after stimulus offset. The presence or absence of these unusual responses on error trials, as well as their magnitude, was affected by the behavioral significance of stimuli used in the task. We hypothesize that these responses represent top-down signals from brain region(s) accessing information about stimuli in the entire visual field and about the behavioral state of the animal. The recruitment of neurons in the opposite hemisphere during processing of behaviorally relevant visual signals reveals a mechanism by which sensory processing can be affected by cognitive task demands.


1991 ◽  
Vol 66 (2) ◽  
pp. 505-529 ◽  
Author(s):  
R. C. Reid ◽  
R. E. Soodak ◽  
R. M. Shapley

1. Simple cells in cat striate cortex were studied with a number of stimulation paradigms to explore the extent to which linear mechanisms determine direction selectivity. For each paradigm, our aim was to predict the selectivity for the direction of moving stimuli given only the responses to stationary stimuli. We have found that the prediction robustly determines the direction and magnitude of the preferred response but overestimates the nonpreferred response. 2. The main paradigm consisted of comparing the responses of simple cells to contrast reversal sinusoidal gratings with their responses to drifting gratings (of the same orientation, contrast, and spatial and temporal frequencies) in both directions of motion. Although it is known that simple cells display spatiotemporally inseparable responses to contrast reversal gratings, this spatiotemporal inseparability is demonstrated here to predict a certain amount of direction selectivity under the assumption that simple cells sum their inputs linearly. 3. The linear prediction of the directional index (DI), a quantitative measure of the degree of direction selectivity, was compared with the measured DI obtained from the responses to drifting gratings. The median value of the ratio of the two was 0.30, indicating that there is a significant nonlinear component to direction selectivity. 4. The absolute magnitudes of the responses to gratings moving in both directions of motion were compared with the linear predictions as well. Whereas the preferred direction response showed only a slight amount of facilitation compared with the linear prediction, there was a significant amount of nonlinear suppression in the nonpreferred direction. 5. Spatiotemporal inseparability was demonstrated also with stationary temporally modulated bars. The time course of response to these bars was different for different positions in the receptive field. The degree of spatiotemporal inseparability measured with sinusoidally modulated bars agreed quantitatively with that measured in experiments with stationary gratings. 6. A linear prediction of the responses to drifting luminance borders was compared with the actual responses. As with the grating experiments, the prediction was qualitatively accurate, giving the correct preferred direction but underestimating the magnitude of direction selectivity observed.(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.


1993 ◽  
Vol 10 (1) ◽  
pp. 93-115 ◽  
Author(s):  
B. Dreher ◽  
A. Michalski ◽  
R. H. T. Ho ◽  
C. W. F. Lee ◽  
W. Burke

AbstractExtracellular recordings from single neurons have been made from presumed area 21a of the cerebral cortex of the cat, anesthetized with N2O/O2/sodium pentobarbitone mixture. Area 21a contains mainly a representation of a central horizontal strip of contralateral visual field about 5 deg above and below the horizontal meridian.Excitatory discharge fields of area 21a neurons were substantially (or slightly but significantly) larger than those of neurons at corresponding eccentricities in areas 17, 19, or 18, respectively. About 95% of area 21a neurons could be activated through either eye and the input from the ipsilateral eye was commonly dominant. Over 90% and less than 10% of neurons had, respectively, C-type and S-type receptive-field organization. Virtually all neurons were orientation-selective and the mean width at half-height of the orientation tuning curves at 52.9 deg was not significantly different from that of neurons in areas 17 and 18. About 30% of area 21a neurons had preferred orientations within 15 deg of the vertical.The mean direction-selectivity index (32.8%) of area 21a neurons was substantially lower than the indices for neurons in areas 17 or 18. Only a few neurons exhibited moderately strong end-zone inhibition. Area 21a neurons responded poorly to fast-moving stimuli and the mean preferred velocity at about 12.5 deg/s was not significantly different from that for area 17 neurons.Selective pressure block of Y fibers in contralateral optic nerve resulted in a small but significant reduction in the preferred velocities of neurons activated via the Y-blocked eye. By contrast, removal of the Y input did not produce significant changes in the spatial organization of receptive fields (S or C type), the size of the discharge fields, the width of orientation tuning curves, or direction-selectivity indices.Our results are consistent with the idea that area 21a receives its principal excitatory input from area 17 and is involved mainly in form rather than motion analysis.


1995 ◽  
Vol 73 (6) ◽  
pp. 2584-2590 ◽  
Author(s):  
G. Cadoret ◽  
A. M. Smith

1. Neurons with proprioceptive or cutaneous receptive fields associated with the hand were identified in the ventral bank of the cingulate sulcus in the monkey. Cells with proprioceptive fields outnumbered cells receiving cutaneous afferents by more than three to one. No cells were encountered that received convergent proprioceptive and cutaneous input. The high concentration of these neurons in the lateral depth of the cingulate sulcus establishes that a distinct hand representation exists within the rostral part of area 23c. 2. Hand-related neurons in area 23c exhibited strong activity modulations during grasping, lifting, and holding an object with the contralateral thumb and index finger. Force pulse perturbations applied to the object elicited excitatory responses at latencies of approximately 45 ms. The modulation of the cellular activity and the input-output properties of these cingulate neurons suggest that, like neurons of primary motor and sensory cortex, these cingulate neurons are also involved in the sensorimotor control of finger movements.


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