Rat thalamic neurons encode complex combinations of heading and movement directions and the trajectory route during translocation with sensory conflict

Abstract

It is unknown how thalamic head direction neurons extract meaningful information from multiple conflicting sensory information sources when animals run under conditions of sensory mismatch. In the present study, rats were placed on a treadmill on a stage that moved in a figure-8-shaped pathway. The anterodorsal and laterodorsal neurons were recorded under two conditions: (1) control sessions, in which both the stage and the treadmill moved forward, or (2) backward (mismatch) sessions, in which the stage was moved backward while the rats ran forward on the treadmill. Of the 222 thalamic neurons recorded, 55 showed differential responses to the directions to window (south) and door (north) sides, along which the animals were translocated in the long axis of the trajectory. Of these 55 direction-related neurons, 15 showed heading direction-dependent responses regardless of movement direction (forward or backward movements). Thirteen neurons displayed heading and movement direction-dependent responses, and, of these 13, activity of 6 neurons increased during forward movement to the window or door side, while activity of the remaining 7 neurons increased during backward movement to the window or door side. Eighteen neurons showed movement direction-related responses regardless of heading direction. Furthermore, activity of some direction-related neurons increased only in a specific trajectory. These results suggested that the activity of these neurons reflects complex combinations of facing direction (landmarks), movement direction (optic flow/vestibular information), motor/proprioceptive information, and the trajectory of the movement.

Do the anterior and lateral thalamic nuclei make distinct contributions to spatial representation and memory?

“…These observations suggest that laterodorsal thalami are additionally influenced by non-visual, local maze cues, which is consistent with the observation that laterodorsal thalamic neurons fire in relation to somatosensory cues such as vibrissae stimulation (Bezdudnaya & Keller, 2008). In addition, a recent report indicated that subpopulations of directional cells in the laterodorsal thalamus fire along specific environmental routes and in specific forward or backward movement directions (Enkhjargal et al, 2014), and experiments using axonal calcium imaging indicate that the lateroposterior thalamus conveys movement related information to cortical regions, including locomotion speed, saccadic-related movements, and optic flow (Roth et al, 2016). Collectively, these observations parallel the diversity of neural firing in the primary input region of the lateral thalamus, the superior colliculus, which reportedly contains neurons that discharge in relation to a number of somatosensory-motor events, including egocentric body turns (e.g., turn left or turn right), and the direction of movement, e.g., toward the center of the maze vs. away from the center (Cooper et al, 1998).…”

Experience-Related Changes in Place Cell Responses to New Sensory Configuration That Does Not Occur in the Natural Environment in the Rat Hippocampus

“…Seven Wistar male rats weighing 200–300 g were used. The animals were similarly treated according to our previous protocols ( Dayawansa et al, 2006 ; Zou et al, 2009 ; Enkhjargal et al, 2014 ). They were individually housed in cages controlled at a constant temperature (20 ± 2°C) with free access to water and laboratory chow.…”

“…Previous studies suggest that theta rhythm is implicated in both the encoding and retrieval of information in the HF ( Hasselmo et al, 2002 ; Manns et al, 2007b ; Terada et al, 2017 ) and also in modulation of HF synaptic current during learning ( Brankack et al, 1993 ; Wyble et al, 2000 ; Orr et al, 2001 ), suggesting that HF theta waves might reflect the activity of a HF comparator during navigation ( Zou et al, 2009 ). In our previous studies, to analyze HF theta rhythm and thalamic head direction cell activity in a mismatch condition, rats locomoted on a treadmill that was translocated along a figure 8-shaped track by a motion stage ( Zou et al, 2009 ; Enkhjargal et al, 2014 ). In a mismatch condition, although rats locomoted forward on the treadmill, the treadmill itself was translocated backward ( Zou et al, 2009 ; Enkhjargal et al, 2014 ).…”

“…In our previous studies, to analyze HF theta rhythm and thalamic head direction cell activity in a mismatch condition, rats locomoted on a treadmill that was translocated along a figure 8-shaped track by a motion stage ( Zou et al, 2009 ; Enkhjargal et al, 2014 ). In a mismatch condition, although rats locomoted forward on the treadmill, the treadmill itself was translocated backward ( Zou et al, 2009 ; Enkhjargal et al, 2014 ). In this mismatch condition, idiothetic sensory inputs (optic flow, vestibular inputs, and proprioceptive inputs or motor efferent copies) contradicted each other (i.e., mismatched); movement direction indicated by the proprioceptive inputs and/or motor efferent copies during locomotion did not match that indicated by the visual-vestibular inputs.…”

For Value or for Worth? Part 1: Speaking Syllogistic Attractors of Appropriations in a Thought-Action-Mood-Space

“…The linguistic thalamus in fact responds to complex permutations [62], transmits cortico-cortically [63], sharpens the focus through the CSTCs, joins cognitive and motor processing [64], chooses words [65] or syntax [66] intending minimized efforts [67]. Direct tracts connect Broca's region to the anterior thalamus [68].…”