The effects of short-term synaptic depression at thalamocortical synapses on orientation tuning in cat V1 (original) (raw)
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Journal of Neuroscience, 2007
Simple cells in layer 4 of the primary visual cortex of the cat show contrast-invariant orientation tuning, in which the amplitude of the peak response is proportional to the stimulus contrast but the width of the tuning curve hardly changes with contrast. This study uses a detailed model of spiny stellate cells (SSCs) from cat area 17 to explain this property. The model integrates our experimental data, including morphological and intrinsic membrane properties and the number and spatial distribution of four major synaptic input sources of the SSC: the dorsal lateral geniculate nucleus (dLGN) and three cortical sources. The model also includes synaptic properties of these inputs. The cortical input served as sources of background activity, and visual stimuli was modeled as sinusoidal grating. For all contrasts, strong synaptic depression of the dLGN feedforward afferents compresses the firing rates in response to orthogonal stimuli, keeping these rates at practically the same low level. However, at preferred orientations, despite synaptic depression, firing rate changes as a function of contrast. Thus, when embedded in an active network, strong synaptic depression can explain contrast-invariant orientation tuning of simple cells. This is true also when the dLGN inputs are partially depressed as a result of their spontaneous activity and to some extent also when parameters were fitted to a more moderate level of synaptic depression. The model response is in close agreement with experimental results, in terms of both output spikes and membrane voltage (amplitude and fluctuations), with reasonable exceptions given that recurrent connections were not incorporated.
Dynamics of the orientation-tuned membrane potential response in cat primary visual cortex
Nature neuroscience, 2001
Neurons in the primary visual cortex are highly selective for stimulus orientation, whereas their thalamic inputs are not. Much controversy has been focused on the mechanism by which cortical orientation selectivity arises. Although an increasing amount of evidence supports a linear model in which orientation selectivity is conferred upon visual cortical cells by the alignment of the receptive fields of their thalamic inputs, the controversy has recently been rekindled with the suggestion that late cortical input--delayed by multiple synapses--could lead to sharpening of orientation selectivity over time. Here we used intracellular recordings in vivo to examine temporal properties of the orientation-selective response to flashed gratings. Bayesian parameter estimation demonstrated that both preferred orientation and tuning width were stable throughout the response to a single stimulus.
Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex
The Journal of Neuroscience, 2005
Neurons in primary visual cortex exhibit several nonlinearities in their responses to visual stimuli, including response decrements to repeated stimuli, contrast-dependent phase advance, contrast saturation, and cross-orientation suppression. Thalamocortical synaptic depression has been implicated in these phenomena but has not been examined directly in visual cortexin vivo. We assessed depression of visual thalamocortical synapsesin vivousing 20-100 Hz trains of electrical stimuli delivered to the LGN. Cortical cells receiving direct input from the LGN, identified by short latency and low jitter of LGN-evoked PSPs, showed moderate reductions in PSP amplitude during the fastest trains. Cells receiving indirect input from the thalamus via other cortical excitatory neurons show a marked reduction in PSP amplitude during a train, which could be explained either by synaptic depression in corticocortical synapses or by an inhibition-mediated suppression of the firing of their afferents. ...
Direction selectivity of synaptic potentials in simple cells of the cat visual cortex
Journal of neurophysiology, 1997
Direction selectivity of synaptic potentials in simple cells of the cat visual cortex. J. Neurophysiol. 78: 2772-2789, 1997. The direction selectivity of simple cells in the visual cortex is generated at least in part by nonlinear mechanisms. If a neuron were spatially linear, its responses to moving stimuli could be predicted accurately from linear combinations of its responses to stationary stimuli presented at different positions within the receptive field. In extracellular recordings, this has not been found to be the case. Although the extracellular experiments demonstrate the presence of a nonlinearity, the cellular process underlying the nonlinearity, whether an early synaptic mechanism such as a shunting inhibition or simply the spike threshold at the output, is not known. To differentiate between these possibilities, we have recorded intracellularly from simple cells of the intact cat with the whole cell patch technique. A linear model of direction selectivity was used to a...
Frontiers in Neuroscience, 2007
Analysis of the timecourse of the orientation tuning of responses in primary visual cortex (V1) can provide insight into the circuitry underlying tuning. Several studies have examined the temporal evolution of orientation selectivity in V1 neurons, but there is no consensus regarding the stability of orientation tuning properties over the timecourse of the response. We have used reverse-correlation analysis of the responses to dynamic grating stimuli to re-examine this issue in cat V1 neurons. We find that the preferred orientation and tuning curve shape are stable in the majority of neurons; however, more than forty percent of cells show a significant change in either preferred orientation or tuning width between early and late portions of the response. To examine the influence of the local cortical circuit connectivity, we analyzed the timecourse of responses as a function of receptive field type, laminar position, and orientation map position. Simple cells are more selective, and reach peak selectivity earlier, than complex cells. There are pronounced laminar differences in the timing of responses: middle layer cells respond faster, deep layer cells have prolonged response decay, and superficial cells are intermediate in timing. The average timing of neurons near and far from pinwheel centers is similar, but there is more variability in the timecourse of responses near pinwheel centers. This result was reproduced in an established network model of V1 operating in a regime of balanced excitatory and inhibitory recurrent connections, confirming previous results. Thus, response dynamics of cortical neurons reflect circuitry based on both vertical and horizontal location within cortical networks.
Synaptic Integration by V1 Neurons Depends on Location within the Orientation Map
Neuron, 2002
diversity in the local structure of the functional map, available data suggest that the extent of local connec-Cambridge, Massachusetts 02139 2 Gillespie, D.C., Lampl, I., Anderson, J.S., and Ferster, D. (2001). manuscript, Carsten Hohnke for providing his Matlab analysis tool-Dynamics of the orientation-tuned membrane potential response in box, and Christine Waite for assistance with the manuscript. This cat primary visual cortex. Nat. Neurosci. 4, 1014-1019. work was supported by a predoctoral fellowship from the Howard Hirsch, J.A., Alonso, J.M., Reid, R.C., and Martinez, L.M. (1998). Hughes Medical Institute (J.S.), a fellowship from MECD, Spain Synaptic integration in striate cortical simple cells. J. Neurosci. 18, (J.M.), and grants from the NIH (M.S.). 9517-9528. Hubel, D.H., and Wiesel, T.H. (1962). Receptive fields, binocular Received: May 21, 2002 interaction and functional architecture of the cat's visual cortex. References tion-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. Cereb. Alonso, J.M., and Martinez, L.M. (1998). Functional connectivity be-Cortex 7, 605-618. tween simple cells and complex cells in cat striate cortex. Nat. Neurosci. 1, 395-403. Knierim, J.J., and van Essen, D.C. (1992). Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. J. Anderson, J.S., Carandini, M., and Ferster, D. (2000a). Orientation Neurophysiol. 67, 961-980. tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909-926. Lampl, I., Anderson, J.S., Gillespie, D.C., and Ferster, D. (2001). Prediction of orientation selectivity from receptive field architecture Anderson, J.S., Lampl, I., Gillespie, D.C., and Ferster, D. (2000b). in simple cells of cat visual cortex. Neuron 30, 263-274. The contribution of noise to contrast invariance of orientation tuning in cat visual cortex. Science 290, 1968-1972. Levitt, J.B., and Lund, J.S. (1997). Contrast dependence of contextual effects in primate visual cortex. Nature 387, 73-76. Azouz, R., and Gray, C.M. (2000). Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons Malach, R., Amir, Y., Harel, M., and Grinvald, A. (1993). Relationship in vivo. Proc. Natl. Acad. Sci. USA 97, 8110-8115. between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate Blasdel, G.G. (1992). Orientation selectivity, preference, and contistriate cortex. Proc. Natl. Acad. Sci. USA 90, 10469-10473. nuity in monkey striate cortex. J. Neurosci. 12, 3139-3161.
The Journal of Physiology, 2011
Non technical summary Neurones of the mammalian primary visual cortex have the remarkable property of being selective for the orientation of visual contours. It has been controversial whether this selectivity arises purely from mechanisms within the cortex itself, from the special way afferents from the thalamus project to the cortex or from the sharpening of a bias for orientation that already exists in the retina and the thalamus. Our experiments support the last of these three hypotheses. We used a special protocol to study both inhibitory and excitatory interactions within the cortex as well as in the thalamus and we find that the orientation selectivity may depend upon multiple mechanisms-including the thalamic biases for orientation and intracortical inhibition and excitation.
Synaptic Plasticity Can Produce and Enhance Direction Selectivity
PLoS Computational Biology, 2005
The discrimination of the direction of movement of sensory images is critical to the control of many animal behaviors. We propose a parsimonious model of motion processing that generates direction selective responses using short-term synaptic depression and can reproduce salient features of direction selectivity found in a population of neurons in the midbrain of the weakly electric fish Eigenmannia virescens. The model achieves direction selectivity with an elementary Reichardt motion detector: information from spatially separated receptive fields converges onto a neuron via dynamically different pathways. In the model, these differences arise from convergence of information through distinct synapses that either exhibit or do not exhibit short-term synaptic depression-short-term depression produces phase-advances relative to nondepressing synapses. Short-term depression is modeled using two state-variables, a fast process with a time constant on the order of tens to hundreds of milliseconds, and a slow process with a time constant on the order of seconds to tens of seconds. These processes correspond to naturally occurring time constants observed at synapses that exhibit short-term depression. Inclusion of the fast process is sufficient for the generation of temporal disparities that are necessary for direction selectivity in the elementary Reichardt circuit. The addition of the slow process can enhance direction selectivity over time for stimuli that are sustained for periods of seconds or more. Transient (i.e., short-duration) stimuli do not evoke the slow process and therefore do not elicit enhanced direction selectivity. The addition of a sustained global, synchronous oscillation in the gamma frequency range can, however, drive the slow process and enhance direction selectivity to transient stimuli. This enhancement effect does not, however, occur for all combinations of model parameters. The ratio of depressing and nondepressing synapses determines the effects of the addition of the global synchronous oscillation on direction selectivity. These ingredients, short-term depression, spatial convergence, and gamma-band oscillations, are ubiquitous in sensory systems and may be used in Reichardt-style circuits for the generation and enhancement of a variety of biologically relevant spatiotemporal computations.