Whisker-related afferents in superior colliculus

Abstract

Rodents use their whiskers to explore the environment, and the superior colliculus is part of the neural circuits that process this sensorimotor information. Cells in the intermediate layers of the superior colliculus integrate trigeminotectal afferents from trigeminal complex and corticotectal afferents from barrel cortex. Using histological methods in mice, we found that trigeminotectal and corticotectal synapses overlap somewhat as they innervate the lower and upper portions of the intermediate granular layer, respectively. Using electrophysiological recordings and optogenetics in anesthetized mice in vivo, we showed that, similar to rats, whisker deflections produce two successive responses that are driven by trigeminotectal and corticotectal afferents. We then employed in vivo and slice experiments to characterize the response properties of these afferents. In vivo, corticotectal responses triggered by electrical stimulation of the barrel cortex evoke activity in the superior colliculus that increases with stimulus intensity and depresses with increasing frequency. In slices from adult mice, optogenetic activation of channelrhodopsin-expressing trigeminotectal and corticotectal fibers revealed that cells in the intermediate layers receive more efficacious trigeminotectal, than corticotectal, synaptic inputs. Moreover, the efficacy of trigeminotectal inputs depresses more strongly with increasing frequency than that of corticotectal inputs. The intermediate layers of superior colliculus appear to be tuned to process strong but infrequent trigeminal inputs and weak but more persistent cortical inputs, which explains features of sensory responsiveness, such as the robust rapid sensory adaptation of whisker responses in the superior colliculus.

AAV-Mediated Anterograde Transsynaptic Tagging: Mapping Corticocollicular Input-Defined Neural Pathways for Defense Behaviors

“…Since the ChR2-labeled V1 axons contained the Cre virus, the functional coupling between the former and the transneuronally labeled striatal neurons provides strong evidence for transsynaptic spread of the Cre virus to synaptically connected target neurons. To further support this notion, our control experiments (Castro-Alamancos and Favero, 2016) demonstrated that the LED-evoked current was only synaptic in nature, as antagonists of glutamate receptors completely blocked the current (Figure S3). …”

Superior colliculus modulates cortical coding of somatosensory information

“…In addition, intermediate and deeper layers of SC also receive sensory information from the whiskers, via a projection from vS1 as well as directly via the trigeminal nucleus of the brainstem 8,20,21 . While several studies have shown that SC neurons are directly activated by whisker deflections 6,22 , it is not known whether activation of SC modulates coding of whisker input in vS1. This issue is the focus of the current study.…”

“…It is well established that SC receives direct input from the primary sensory cortices [4][5][6][7][8][9] . What is less clear is whether SC, in turn, modulates information processing in the cortex.…”

Superior colliculus modulates cortical coding of somatosensory information

“…It is well established that SC receives direct input from the primary sensory cortices (Welker et al, 1988;May, 2006;Cohen et al, 2008;Triplett et al, 2012;Castro-Alamancos & Favero, 2016;Zingg et al, 2017). What is less clear is whether SC in turn modulates information processing in the cortex.…”

“…Sensory information from the whiskers is processed by the whisker associated area of the somatosensory cortex, known as the primary vibrissal somatosensory cortex (vS1 ;Brecht 2007;Diamond & Arabzadeh 2013). In addition, intermediate and deeper layers of SC also receive sensory information from the whiskers, via a projection from vS1 as well as directly via the trigeminal nucleus of the brainstem (Wise & Jones, 1977;Killackey & Erzurumlu, 1981;Bosman et al, 2011;Triplett et al, 2012;Castro-Alamancos & Favero, 2016). While several studies have shown that SC neurons are directly activated by whisker deflections (Dräger & Hubel, 1976;Castro-Alamancos & Favero, 2016), it is not known whether activation of SC modulates coding of whisker input in vS1.…”