Functional alignment of feedback effects from visual cortex to thalamus (original) (raw)

Focal Gain Control of Thalamic Visual Receptive Fields by Layer 6 Corticothalamic Feedback

Cerebral cortex (New York, N.Y. : 1991), 2016

The projections between the thalamus and primary visual cortex (V1) are a key reciprocal neural circuit, relaying retinal signals to cortical layers 4 & 6 while being simultaneously regulated by massive layer 6 corticothalamic feedback. Effectively dissecting the influence of this corticothalamic feedback circuit in higher mammals remains a challenge for vision research. By pharmacologically increasing the focal gain of visually driven layer 6 responses of cat V1 in a controlled fashion, we examined the effects of such focal cortical changes on the response amplitudes and spatial structure of the receptive fields (RFs) of individual dorsal lateral geniculate nucleus (dLGN) cells. We found that enhancing visually driven cortical feedback could facilitate or suppress the overall responses of dLGN cells, and such an effect was linked to the orientation preference of the cortical neuron. Related to these selective retinotopic gain changes, enhanced feedback induced the RFs of dLGN cells...

Thalamocortical Specificity and the Synthesis of Sensory Cortical Receptive Fields

Alonso, Jose-Manuel and Harvey A. Swadlow. Thalamocortical specificity and the synthesis of sensory cortical receptive fields. . A persistent and fundamental question in sensory cortical physiology concerns the manner in which receptive fields of layer-4 neurons are synthesized from their thalamic inputs. According to a hierarchical model proposed more than 40 years ago, simple receptive fields in layer 4 of primary visual cortex originate from the convergence of highly specific thalamocortical inputs (e.g., geniculate inputs with ON-center receptive fields overlap the ON subregions of layer 4 simple cells).

Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex

Nature Neuroscience, 2011

The primary visual cortex of primates and carnivores is organized into columns of neurons with similar preferences for stimulus orientation, but the developmental origin and function of this organization are still matters of debate. We found that the orientation preference of a cortical column is closely related to the population receptive field of its ON and OFF thalamic inputs. The receptive field scatter from the thalamic inputs was more limited than previously thought and matched the average receptive field size of neurons at the input layers of cortex. Moreover, the thalamic population receptive field (calculated as ON -OFF average) had separate ON and OFF subregions, similar to cortical neurons in layer 4, and provided an accurate prediction of the preferred orientation of the column. These results support developmental models of orientation maps that are based on the receptive field arrangement of ON and OFF visual inputs to cortex.

Differential Feedback Modulation of Center and Surround Mechanisms in Parvocellular Cells in the Visual Thalamus

Journal of Neuroscience, 2012

where the response to a centrally placed stimulus is modified when a surrounding area is also stimulated. This can follow from laterally directed connections in the local circuit at the level of the cell in question but could also involve more complex interactions. In the lateral geniculate nucleus (LGN), the cells relaying the retinal input display a concentric, center surround organization that in part follows from the similar organization characterizing the retinal cells providing their input. However, local thalamic inhibitory interneurons also play a role, and as we examine here, feedback from the visual cortex too. Here, we show in the primate (macaque) that spatially organized cortical feedback provides a clear and differential influence serving to enhance both responses to stimulation within the center of the receptive field and the ability of the nonclassical surround mechanism to attenuate this. In short, both center and surround mechanisms are influenced by the feedback. This dynamically sharpens the spatial focus of the receptive field and introduces nonlinearities from the cortical mechanism into the LGN.

Visual Orientation and Directional Selectivity through Thalamic Synchrony

Journal of Neuroscience, 2012

Thalamic neurons respond to visual scenes by generating synchronous spike trains on the timescale of 10 -20 ms that are very effective at driving cortical targets. Here we demonstrate that this synchronous activity contains unexpectedly rich information about fundamental properties of visual stimuli. We report that the occurrence of synchronous firing of cat thalamic cells with highly overlapping receptive fields is strongly sensitive to the orientation and the direction of motion of the visual stimulus. We show that this stimulus selectivity is robust, remaining relatively unchanged under different contrasts and temporal frequencies (stimulus velocities). A computational analysis based on an integrate-and-fire model of the direct thalamic input to a layer 4 cortical cell reveals a strong correlation between the degree of thalamic synchrony and the nonlinear relationship between cortical membrane potential and the resultant firing rate. Together, these findings suggest a novel population code in the synchronous firing of neurons in the early visual pathway that could serve as the substrate for establishing cortical representations of the visual scene.

Spatial dynamics of receptive fields in cat primary visual cortex related to the temporal structure of thalamocortical feedforward activity

Experimental Brain Research, 2002

We investigated how changes in the temporal firing rate of thalamocortical activity affect the spatiotemporal structure of receptive field (RF) subunits in cat primary visual cortex. Spike activity of 67 neurons (48 simple, 19 complex cells) was extracellulary recorded from area 17/18 of anesthetized and paralyzed cats. A total of 107 subfields (on/off) were mapped by applying a reverse correlation technique to the activity elicited by bright and dark rectangles flashed for 300 ms in a 20×10 grid. We found that the width of the (suprathreshold) discharge fields shrank on average by 22% during this 300-ms-long stimulus presentation time. Fifty-eight subfields (54%) shrank by more than 20% of peak width and only ten (less than 10%) showed a slight increase over time. The main size reduction took place 40-60 ms after response onset, which corresponded to the transition from transient peak firing to tonic visual activity in thalamocortical relay cells (TC). The experimentally obtained RFs were then fitted with the aid of a neural field model of the primary visual pathway. Assuming a Gaussian-shaped spatial sensitivity profile across the RF subfield width, the model allowed us to estimate the subthreshold RF (depolarization field, D-field) from the minimal discharge field (MDF). The model allowed us to test to what degree the temporal dynamics of thalamocortical activity contributes to the spatiotemporal changes of cortical RFs. To this end, we performed the fitting procedure either with a pure feedforward model or with a field model that also included intracortical feedback. Spatial and temporal parameters obtained from fits of the experimental RFs matched closely to those achieved by simulating a pure feedforward system with the field model but were not compatible with additional intracortical feedback. Thus, our results show that dot stimulation, which optimally excites thalamocortical cells, leads to a shrinkage with respect to the size of the RF subfield at the first transient response of visual cortical RFs which seems mainly due to a change in the thalamic firing pattern. In these experiments little or no influence from intracortical sources was observed, which, however, may play a role when using more complex visual stimuli. Keywords Thalamocortical response dynamics • Cortical spatiotemporal receptive field dynamics • Field model • Depolarization field • Discharge field • Cat

Cortical direction selectivity emerges at convergence of thalamic synapses

Nature, 2018

Detecting the direction of an object's motion is essential for our representation of the visual environment. Visual cortex is one of the main stages in the mammalian nervous system where motion direction may be computed de novo. Experiments and theories indicate that cortical neurons respond selectively to motion direction by combining inputs that provide information about distinct spatial locations with distinct time-delays. Despite the importance of this spatiotemporal offset for direction selectivity its origin and cellular mechanisms are not fully understood. We show that ~80+/-10 thalamic neurons responding with distinct time-courses to stimuli in distinct locations contribute to the excitation of mouse visual cortical neurons during visual stimulation. Integration of thalamic inputs with the appropriate spatiotemporal offset provides cortical neurons with the primordial bias for direction selectivity. These data show how cortical neurons selectively combine the spatiotemporal response diversity of thalamic neurons to extract fundamental features of the visual world. The ability to detect the direction of motion of objects in the visual world is an essential property of sensory processing. In the primary visual cortex of mammals many neurons preferentially respond to stimuli moving in a specific direction within their receptive field 1,2. In primates and carnivores, this sensitivity to motion direction is believed not to be inherited from earlier stages of visual processing but computed de novo in visual cortex. Here, neurons likely extract directional motion from the visual scene

Tuned thalamic excitation is amplified by visual cortical circuits

Nature Neuroscience, 2013

Cortical neurons in thalamic recipient layers receive excitation from the thalamus and the cortex. The relative contribution of these two sources of excitation to sensory tuning is poorly understood. Here we optogenetically silence the visual cortex of mice to isolate thalamic excitation onto layer 4 neurons during visual stimulation. Thalamic excitation contributes to a third of total excitation and is organized in spatially offset, yet overlapping ON and OFF receptive fields. This receptive field structure predicts the orientation tuning of thalamic excitation. Finally, thalamic and total excitation are similarly tuned to orientation and direction, and have the same temporal phase relationship to the visual stimulus. Our results indicate that tuning of thalamic excitation is unlikely to be imparted by direction or orientation selective thalamic neurons and that a principal role of cortical circuits is to amplify tuned thalamic excitation. Users may view, print, copy, download and text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial\_policies/license.html#terms Author Contributions A.D.L. and M.S. designed the study. A.D.L. conducted all experiments and analysis. A.D.L. and M.S. wrote the paper.