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

Abstract

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. O rientation selective neurons in primary visual cortex receive feed-forward input from lateral geniculate nucleus (LGN) cells that are themselves poorly oriented. Experiments that have examined the role of the feed-forward thalamocortical pathway in this receptive field transformation have yielded two independent findings. First, the thalamic input to cortical simple cells is highly specific; LGN cells make monosynaptic connections with simple cells predominantly when the pre-and postsynaptic receptive fields overlap and match in sign, size, and time course (1, 2). Second, when intracortical inputs are silenced by cooling or by electrical stimulation in cortex, intracellular recordings demonstrate that the summed thalamic input to a layer 4 simple cell is orientation selective (3, 4). Here, we present a technique that we have used to examine a related but hitherto untested hypothesis: that the spatial receptive field of a simple cell is very similar to the receptive field of its summed thalamic input. We have concentrated on two receptive-field parameters, the elongation of the strongest subfield and the relative strength of antagonistic, flanking subfields.The experimental approach that we took to examine these questions was based on two independent characteristics of electrical stimulation: (i) if electrical stimulation is not 100% effective in evoking cortical spikes, then the probability of evoking a spike will depend on the subthreshold activity of the cortical neuron at the time of the stimulus, and (ii) strong electrical stimulation leads to prolonged (...

Unravelling cerebellar pathways with high temporal precision targeting motor and extensive sensory and parietal networks

“…Stimulation of the neocortex revealed the presence of strong inhibition, thus preventing the propagation of electrically induced activation over multi-synaptic pathways. Th is is in good agreement with the prominence of inhibition both in its duration 10,53 and in the presence of a wealth of diff erent inhibitory interneurons in the neocortex 54 . Comparable inhibitory mechanisms do not seem to matter in the case of stimulation of the cerebellar output.…”

Regulation of spike timing in visual cortical circuits

“…Thalamocortical synapses are more effective than intracortical synapses 94 , but they form only a small fraction of the synapses onto SSCs 95,96 . Nevertheless, collectively they seem to be efficient in driving the SSCs 45,97 . The reason for this efficiency was elucidated in another cortical area, in neurons that project from the ventroposteromedial thalamus (VPM) to the barrel cortex 98 and that respond to whisker movement.…”

“…Neurons in layer 4 of the primary visual cortex can also fire with high precision in response to visual inputs 45,46 . Neurons in the mediotemporal cortex in turn receive inputs from the primary visual cortex and respond to motion.…”

“…When recordings from cells of the same type in different animals were compared, most of the events occurred at similar times during the stimulus presentation 43 . It is likely, therefore, that in the same animal multiple neurons produce spikes at similar times, resulting in synchronous volleys to the primary visual cortex 44 .Neurons in layer 4 of the primary visual cortex can also fire with high precision in response to visual inputs 45,46 . Neurons in the mediotemporal cortex in turn receive inputs from the primary visual cortex and respond to motion.…”

Short-Term Depression in Thalamocortical Synapses of Cat Primary Visual Cortex

“…Whereas field potential recordings suggest substantial geniculocortical depression in the rat (Jia et al, 2004), extracellular studies in the cat found facilitation of spike efficacy in response to LGN spikes elicited at short intervals (Usrey et al, 2000). Additionally, responses to electrical stimulation of the LGN are facilitated during and after the presentation of a visual stimulus (Kara et al, 2002).…”