Behavioral State Dependency of Neural Activity and Sensory (Whisker) Responses in Superior Colliculus

Abstract

Rats use their vibrissa (whiskers) to explore and navigate the environment. These sensory signals are distributed within the brain stem by the trigeminal complex and are also relayed to the superior colliculus in the midbrain and to the thalamus (and subsequently barrel cortex) in the forebrain. In the intermediate layers of the superior colliculus, whisker-evoked responses are driven by direct inputs from the trigeminal complex (trigeminotectal) and feedback from the barrel cortex (corticotectal). But the effects of the behavioral state of the animal on the spontaneous firing and sensory responses of these neurons are unknown. By recording from freely behaving rats, we show that the spontaneous firing of whisker sensitive neurons in superior colliculus is higher, or in an activated mode, during active exploration and paradoxical sleep and much lower, or in a quiescent/deactivated mode, during awake immobility and slow-wave sleep. Sensory evoked responses in superior colliculus also depend on behavioral state. Most notably, feedback corticotectal responses are significantly larger during the quiescent/deactivated mode, which tracks the barrel cortex responses on which they depend. Finally, sensory evoked responses depend not only on the state of the animal but also on the orienting response elicited by the stimulus, which agrees with the well known role of the superior colliculus in orienting about salient stimuli.

Superior colliculus cells sensitive to active touch and texture during whisking

“…This is a feature shared by other ascending sensory pathways, such as the trigeminothalamic pathway, and is known to be highly sensitive to behavioral state and neuromodulator influences (Castro-Alamancos 2002a, 2002b, 2004b. In fact, recent work has shown that whisker-sensitive cells in the superior colliculus are highly sensitive to changes in behavioral state (Cohen and Castro-Alamancos 2010a). Moreover, neuromodulators, such as acetylcholine, norepinephrine, and serotonin, are released in the superior colliculus during specific states and are likely to affect whisking and active touch signals.…”

“…In the superior colliculus, we measured spike probability during a long time window (2-80 ms poststimulus) or several short time windows. Peak1 (2-10 ms), peak2 (11-20 ms), and peak3 (21-80 ms) time window responses were calculated because they reflect responses of different origins and with different sensitivities to behavior (Cohen and Castro-Alamancos 2010a, 2010b, 2010cCohen et al 2008). All data are expressed as means Ϯ SE unless otherwise stated.…”

“…Superior colliculus passive touch responses are driven by direct inputs from the trigeminal complex (trigeminotectal; peak1) followed by activity returning from the barrel cortex (corticotectal; peak2) in both anesthetized (Cohen et al 2008) and freely behaving rats (Cohen and Castro-Alamancos 2010a). However, the superior colliculus responses produced by active touch (i.e., whisking on objects) are unknown.…”

A new view of “dream enactment” in REM sleep behavior disorder

“…Therefore, we propose further that RBD entails disinhibition of neural circuits that contribute to the production of defensive and aggressive behaviors, including but not limited to the superior colliculus. In support of this proposal, cholinergic neurons in the laterodorsal tegmental nucleus and the pedunculopontine tegmental nucleus, which are vulnerable to degeneration in the α-synucleinopathies [81,82], project to the superior colliculus [83,84] and may modulate its activity [85]. …”

Activation of Retinotopic Visual Areas Is Central to REM Sleep Associated Dreams: Visual Dreams and Visual Imagery Possibly Co-Emerged In Evolution

“…Therefore, in higher species it possibly acquired new roles including multisensory integration (Alvarado et al, 2009) for example and visual information processing is most important function of this area. The visual system, particularly the retinotopic SC-circuit (Chan et al, 2011), is intensely activated during REMS (Cohen & Castro-Alamancos, 2010), and all dreams essentially have visual experiences (Nir & Tononi, 2010). Sprenger et al (2010) recently studied kinematic parameters of REMs during REMS and suggested that REMs may be related to exploratory saccadic behavior during awake to remember visual stimuli.…”