The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation (original) (raw)

Faculty of 1000 evaluation for The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation

F1000 - Post-publication peer review of the biomedical literature, 2002

Electrical stimulation of the thalamus has been widely used to test for the existence of monosynaptic input to cortical neurons, typically with stimulation currents that evoke cortical spikes with high probability. We stimulated the lateral geniculate nucleus (LGN) of the thalamus and recorded monosynaptically evoked spikes from layer 4 neurons in visual cortex. We found that with moderate currents, cortical spikes were evoked with low to moderate probability and their occurrence was modulated by ongoing sensory (visual) input. Furthermore, when repeated at 8-12 Hz, electrical stimulation of the thalamic afferents caused such profound inhibition that cortical spiking activity was suppressed, aside from electrically evoked monosynaptic spikes. Visual input to layer 4 cortical cells between electrical stimuli must therefore have derived exclusively from LGN afferents. We used white-noise visual stimuli to make a 2D map of the receptive field of each cortical simple cell during repetitive electrical stimulation in the LGN. The receptive field of electrically evoked monosynaptic spikes (and thus of the thalamic input alone) was significantly elongated. Its primary subfield was comparable to that of the control receptive field, but secondary (flanking) subfields were weaker. These findings extend previous results from intracellular recordings, but also demonstrate the effectiveness of an extracellular method of measuring subthreshold afferent input to cortex.

Activation of a cortical column by a thalamocortical impulse

The Journal of …, 2002

Thalamocortical (TC) impulses potently influence the sensory neocortex, but the functional impact of individual TC neurons throughout the layers of the cortex has proved difficult to assess. Here we examine, in awake rabbits, the vertical distribution of monosynaptic currents generated in a somatosensory cortical "barrel" column by spontaneous impulses of single, topographically aligned TC neurons. We show that closely neighboring TC neurons generate widely differing patterns of monosynaptic activation within layers 4 and 6 of their aligned column. Moreover, synaptic currents generated by TC impulses with long preceding interspike intervals are greatly enhanced in both of these layers. The degree of this enhancement differs reliably among neighboring TC neurons but, for a given neuron, is very similar in layers 4 and 6. Our results indicate that in the awake state, TC synapses throughout the depth of the cortex serve as powerful filters of sensory information that reflect individual characteristics of their parent TC neuron.

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).

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.

Spatiotemporal Gating of Sensory Inputs in Thalamus during Quiescent and Activated States

The Journal of Neuroscience, 2005

The main role of the thalamus is to relay sensory inputs to the neocortex according to the regulations dictated by behavioral state. Hence, changes in behavioral state are likely to transform the temporal and spatial properties of thalamocortical receptive fields. We compared the receptive fields of single cells in the ventroposterior medial thalamus (VPM) of urethane-anesthetized rats during quiescent states and during aroused (activated) states. During quiescent states, VPM cells respond to stimulation of a principal whisker (PW) and may respond modestly to one or a few adjacent whiskers (AWs). During either generalized forebrain activation or selective thalamic activation caused by carbachol infusion in the VPM, the responses to AWs enhance so that VPM receptive fields become much larger. Such enlargement is not observed at the level of the principal trigeminal nucleus, indicating that it originates within the thalamus. Interestingly, despite the increase in AW responses during a...

Local and thalamic origins of correlated ongoing and sensory-evoked cortical activities

Nature Communications, 2016

Thalamic inputs of cells in sensory cortices are outnumbered by local connections. Thus, it was suggested that robust sensory response in layer 4 emerges due to synchronized thalamic activity. To investigate the role of both inputs in the generation of correlated cortical activities, we isolated the thalamic excitatory inputs of cortical cells by optogenetically silencing cortical firing. In anaesthetized mice, we measured the correlation between isolated thalamic synaptic inputs of simultaneously patched nearby layer 4 cells of the barrel cortex. Here we report that in contrast to correlated activity of excitatory synaptic inputs in the intact cortex, isolated thalamic inputs exhibit lower variability and asynchronous spontaneous and sensory-evoked inputs. These results are further supported in awake mice when we recorded the excitatory inputs of individual cortical cells simultaneously with the local field potential in a nearby site. Our results therefore indicate that cortical synchronization emerges by intracortical coupling.

Single-neuron interactions between the somatosensory thalamo-cortical circuits during perception

SUMMARYSensory thalamo-cortical interactions are key components of the neuronal chains associated with stimulus perception, but surprisingly, they are poorly understood. We addressed this problem by evaluating a directional measure between simultaneously recorded neurons from somatosensory thalamus (VPL) and somatosensory cortex (S1) sharing the same cutaneous receptive field, while monkeys judged the presence or absence of a tactile stimulus. During the stimulus-presence, feedforward (VPL→S1) interactions increased, while pure feedback (S1→VPL) interactions were unaffected. Remarkably, bidirectional interactions (VPL↔S1) emerged with high stimulus amplitude, establishing a functional thalamo-cortical loop. Furthermore, feedforward interactions were modulated by task context and error trials. Additionally, significant stimulus modulations were found on intra-cortical (S1→S1) interactions, but not on intra-thalamic (VPL→VPL) interactions. Thus, these results show the directionality o...

Synaptic Contributions to Receptive Field Structure and Response Properties in the Rodent Lateral Geniculate Nucleus of the Thalamus

The Journal of neuroscience : the official journal of the Society for Neuroscience, 2016

Comparative physiological and anatomical studies have greatly advanced our understanding of sensory systems. Many lines of evidence show that the murine lateral geniculate nucleus (LGN) has unique attributes, compared with other species such as cat and monkey. For example, in rodent, thalamic receptive field structure is markedly diverse, and many cells are sensitive to stimulus orientation and direction. To explore shared and different strategies of synaptic integration across species, we made whole-cell recordings in vivo from the murine LGN during the presentation of visual stimuli, analyzed the results with different computational approaches, and compared our findings with those from cat. As for carnivores, murine cells with classical center-surround receptive fields had a "push-pull" structure of excitation and inhibition within a given On or Off subregion. These cells compose the largest single population in the murine LGN (∼40%), indicating that push-pull is key in ...

Distinct cortical responses evoked by electrical stimulation of the thalamic ventral intermediate nucleus and of the subthalamic nucleus

NeuroImage: Clinical

To investigate the spatial and temporal pattern of cortical responses evoked by deep brain stimulation (DBS) of the subthalamic nucleus (STN) and ventral intermediate nucleus of the thalamus (VIM). Methods: We investigated 7 patients suffering from Essential tremor (ET) and 7 patients with Parkinson's Disease (PD) following the implantation of DBS electrodes (VIM for ET patients, STN for PD patients). Magnetoencephalography (MEG) was used to record cortical responses evoked by electric stimuli that were applied via the DBS electrode in trains of 5 Hz. Dipole fitting was applied to reconstruct the origin of evoked responses. Results: Both VIM and STN DBS led to short latency cortical responses at about 1 ms. The pattern of medium and long latency cortical responses following VIM DBS consisted of peaks at 13, 40, 77, and 116 ms. The associated equivalent dipoles were localized within the central sulcus, 3 patients showed an additional response in the cerebellum at 56 ms. STN DBS evoked cortical responses peaking at 4 ms, 11 ms, and 27 ms, respectively. While most dipoles were localized in the pre-or postcentral gyrus, the distribution was less homogenous compared to VIM stimulation and partially included prefrontal brain areas. Conclusion: MEG enables localization of cortical responses evoked by DBS of the VIM and the STN, especially in the sensorimotor cortex. Short latency responses of 1 ms suggest cortical modulation which bypasses synaptic transmission, i.e. antidromic activation of corticofugal fiber pathways.