Completing the Corticofugal Loop: A Visual Role for the Corticogeniculate Type 1 Metabotropic Glutamate Receptor

Abstract

The way in which the brain deals with sensory information relies not only on feedforward processing of signals from the periphery but also on feedback inputs. This is the case of the massive projection back from layer 6 in the visual cortex to the thalamus, for which, despite being the greatest single source of synaptic contacts, the functional role still remains unclear. In the cat lateral geniculate nucleus, part of this cortical feedback is mediated by type 1 metabotropic glutamate receptors (mGluR1s), which are exclusively located on distal segments of the relay-cell dendrites. Here we show that in adult cats the cortex uses a synaptic drive mediated by these receptors (mGluR1) specifically to enhance the excitatory center of the thalamic receptive field. Moreover the effect is maximum in response to those stimuli that effectively drive cortical cells, and importantly, it does not affect the spatiotemporal structure of the thalamic receptive field. Therefore, cortex, by closing this corticofugal "loop," is able to increase the gain of its thalamic input within a focal spatial window, selecting key features of the incoming signal.

Corticothalamic feedback enhances stimulus response precision in the visual system

“…In comparison with retinal ganglion cells, LGN cells are known to exhibit lower background and stimulus-driven firing, nonlinear changes in contrast gain and spatial properties, and enhanced center surround antagonism (44)(45)(46)(47)(48). The feedback projection to the LGN has been shown to be involved in these effects (14,(49)(50)(51). Additionally, both the temporal response profile (8,52) and information transfer (10), as well as non-stimulus-locked synchrony (11), are known to be modified by cortical feedback.…”

Learning and inference in the brain

“…In the cat lateral geniculate nucleus, cortical feedback is partly mediated by type 1 metabotropic glutamate receptors, which are located exclusively on distal segments of the relay-cell dendrites. Rivadulla, Martinez, Varela, and Cudeiro (2002) have shown that these backward afferents enhance the excitatory centre of the thalamic receptive field. "Therefore, cortex, by closing this corticofugal loop, is able to increase the gain of its thalamic input within a focal spatial window, selecting key features of the incoming signal" (Rivadulla et al, 2002).…”

Glutamate receptor functions in sensory relay in the thalamus

“…There seems to be little evidence for a contribution to sensory responses of additional glutamate receptors from in vitro physiological studies, even though experiments have been designed that have attempted to reveal roles for, for example, metabotropic glutamate receptors (Turner & Salt 1998). By contrast, the situation appears to differ in in vivo experiments, where there appear to be sensory responses that have a contribution from mGlu receptors, and it is prob- 2002) able that this re ects recruitment of additional circuitry, possibly corticothalamic inputs (see § 3) (Eaton et al 1993;Salt & Turner 1998b;Rivadulla et al 2002).…”

“…This may not be the case in all situations. However, using certain natural somatosensory or visual stimuli which may appropriately activate cortical areas in vivo it has been shown that thalamic responses to sensory stimuli are reduced in the presence of mGlu1 antagonists in both VB ( gure 3) (Salt & Turner 1998b) and the LGN ( gure 4) (Rivadulla et al 2002), and this may re ect activation of the cortical input to the thalamic relay neurons. A feature of some of these stimuli is that they are of a sustained nature, and it may be the case that this is critical to (Rivadulla et al 2002).…”

“…However, using certain natural somatosensory or visual stimuli which may appropriately activate cortical areas in vivo it has been shown that thalamic responses to sensory stimuli are reduced in the presence of mGlu1 antagonists in both VB ( gure 3) (Salt & Turner 1998b) and the LGN ( gure 4) (Rivadulla et al 2002), and this may re ect activation of the cortical input to the thalamic relay neurons. A feature of some of these stimuli is that they are of a sustained nature, and it may be the case that this is critical to (Rivadulla et al 2002). The histograms illustrate the response of an on-centre 'X' cell to a full-eld sinusoidal drifting grating (inset above the histogram) of optimal characteristics (a) before and (b) in the presence of the antagonist LY367385 (ejected iontophoretically using 60 nA for 6 min), and (c) after a recovery period of 15 min.…”