RT Journal Article
SR Electronic
T1 Population temporal structure supplements the rate code during sensorimotor transformations
JF bioRxiv
FD Cold Spring Harbor Laboratory
SP 132514
DO 10.1101/132514
A1 Uday K. Jagadisan
A1 Neeraj J. Gandhi
YR 2017
UL http://biorxiv.org/content/early/2017/05/02/132514.abstract
AB In order to successfully interact with the environment the brain must funnel down the sensory inputs it receives to specific movements at specific times. Such sensory-to-motor transformations are critically mediated by neurons in premotor brain networks whose evolving activities represent sensory, cognitive, and movement-related information1-3. However, this multiplexing poses a conundrum – how does a decoder know precisely when to initiate a movement if such neurons are also active at times other than when a movement occurs (e.g., in response to sensory stimulation)? Extant models of movement generation that rely on firing rate, including rise-to-threshold4, inhibitory gating5, and dynamical switches at the population level6,7, leave certain explanatory gaps unfilled. Here, we propose a novel hypothesis: movement is triggered not only by an increase in firing rate, but critically by a reliable temporal pattern in the population response. We show that in brain regions involved in orienting eye movements - the superior colliculus (SC) and the frontal eye fields (FEF) - the temporal dynamics between neurons during visually-driven activity is different from that during pre-movement activation. Specifically, using a measure that captures the fidelity of the population code - here called temporal stability - we show that the temporal structure fluctuates in the visual response but remains stable during the pre-movement response, thus distinguishing incoming sensory input from motor output. This is an important attribute because SC and FEF “visuomovement” neurons project directly to the brainstem8,9 which houses the controller for gaze shifts, and any increase in the incoming drive is poised to trigger a (potentially undesirable) gaze shift. We also demonstrate that a simple firing rate-based network with synaptic facilitation can distinguish between stable and fluctuating population codes, suggesting a putative mechanism for interpreting temporal structure. These findings offer an alternative perspective on the relationship between spatial attention and motor preparation10,11 by situating the correlates of movement initiation in the temporal features of activity in shared neural substrates. They also suggest a need to look beyond the instantaneous rate code and consider the effects of short-term population history on neuronal communication and its effects on behavior.