Invited Review Anatomical loops and their electrical dynamics in relation to whisking by rat

Abstract

An accumulation of anatomical, behavioral, and electrophysiological evidence allows us to identify the neuronal circuitry that is involved with vibrissa-mediated sensation and the control of rhythmic vibrissa movement. Anatomical evidence points to a multiplicity of closed sensorimotor loops, while electrophysiological data delineate the flow of electrical signals in these pathways. These loops process sensory input from the vibrissae and send projections to direct vibrissa movement, starting at the level of the hindbrain and proceeding toward loops that involve multiple structures in the forebrain. The nature of the vibrissa-related electrical signals in behaving animals has been studied extensively at the level of neocortical loops. Two types of spike signal are observed that serve as a reference of vibrissa motion: a fast signal that correlates with the relative phase of the vibrissae within a whisk cycle and a slow signal that correlates with the amplitude, and possibly the set-point, of the vibrissae during a whisk. Both signals are observed in vibrissa primary sensory (S1) cortex, and in some cases they are sufficiently robust to allow vibrissa position to be accurately estimated from the spike train of a single neuron. Unlike the case for S1 cortex, only the slow signal has been observed in vibrissa primary motor (M1) cortex. The control capabilities of M1 cortex were estimated from experiments with anesthetized animals in which progressive areas along the vibrissa motor branch were microstimulated with rhythm ically applied currents. The motion of the vibrissae followed stimulation of M1 cortex only for rates that were well below the frequency of rhythmic whisking; in contrast, the vibrissae followed stimulation of the facial nucleus, whose cells directly drive the vibrissae, for rates above that of whisking. In toto, the evidence implies that there is fast signaling from the facial nucleus, through the mystacial pad and the vibrissae and up through sensory cortex, but only slow signaling at the level of the motor cortex and down through the superior colliculus to the facial nucleus. The transformation from fast sensory signals to slow motor control is an unresolved issue. On the other hand, there is a candidate scheme to understand how the fast reference of vibrissa motion in the whisk cycle may be used to decode the angle of the vibrissae upon their contact with an object. We discuss a circuit in which servo mechanisms are used to determine the angle of contact relative to the preferred phase of the fast reference signals. Support for this scheme comes from results with anesthetized animals on the frequency and phase entrainment of intrinsic neuronal oscillators in S1 cortex. A prediction based on this scheme is that the output from a decoder circuit is maximal when the angle of contact differs from the preferred phase of a fast regerence signal. In contrast, for correlation-based schemes the output is maximal when the angle of contact equals the preferred phase.

Goal-directed whisking increases phase-locking between vibrissa movement and electrical activity in primary sensory cortex in rat

“…It is conjectured that a central role of vibrissa primary sensory cortex is to compute the position of contact of the vibrissae with tactile stimuli in head-centered coordinates (16,17,40). This computation requires a reference signal of vibrissa position (7,41).…”

A novel method of head fixation for the study of rodent facial function

“…The rodent vibrissial system has been an extremely valuable model for studies attempting to elucidate mechanisms of learning, processing sensory information, and understanding facial sensorimotor reflexes and pathways (Bermejo et al 1996,Nguyen et al 2005,Crish et al 2003,Ahissar et al 2003,Kleinfeld et al 1999. The rodent eye blink model has also been employed to elucidate the relationships between the 5 th and 7 th cranial nerves (Gong et al 2003,Zerari-Mailly et al 2003.…”

Is there a brainstem substrate for action selection?

“…Many of these links have been demonstrated anatomically: direct inputs have been traced from secondary nuclei in the whisker (Kleinfeld et al 1999), auditory (Cant & Benson 2003) and vestibular systems ( Yates & Stocker 1998); the proprioceptive information carried by the ascending dorsal column is directly relayed to the mRF via collaterals from the gracile and cuneate nuclei (Salibi et al 1980); and the spinoreticular tract and collaterals from the spinothalamic tract, the primary routes for pain signals to the brain, are a major source of fibres reaching the mRF (Fields & Basbaum 1978).…”