Cortical and Subcortical Contributions to Short-Term Memory for Orienting Movements.
Charles D. Kopec, Jeffrey C. Erlich, Bingni W. Brunton, Karl Deisseroth, and Carlos D. Brody, Neuron 2015
Short-term memory is an essential higher cognitive function, allowing us to mentally store information, and thereby separate sensory input from motor output. Previous work from a former postdoc in the Brody Lab Jeff Erlich et al. 2011 demonstrated a role for a region of rat prefrontal cortex, the Frontal Orienting Field (FOF), in orienting movements guided by short-term memory. Guided by previous neural recordings conducted in the rat FOF during a simple memory guided orienting task, we sought to test the hypothesis that activity in the rat FOF is causally maintaining the rat’s choice for its upcoming motor act.
Here we used optogenetic inactivation (enhanced Halorhodopsin, eNpHR3.0) to transiently inactivate the FOF during the memory guided orienting task. We predicted that inactivation during the sensory cue, when the FOF is encoding little to no information, should result in little to no bias, while inactivation during the memory delay period, when the FOF in maximally encoding the rat’s decision, should result in a large perturbation of their choice. However, we found precisely the opposite pattern. As information encoded in the FOF increased, the ability to perturb the rat’s choice by disrupting that information decreased. We conducted the same experiments on the deep motor layers of the superior colliculus (SC) and found nearly identical results.
In order to reconcile these seemingly contradictory optogenetic and electrophysiological results we adapted a simple mutually inhibiting dynamical attractor network model. We hypothesize that the network responsible for maintaining the short-term memory for orienting movements is distributed across multiple brain areas including but not limited to the FOF and SC. At the start of a trial the network resides on the unstable hill separating two basins of attraction representing the two alternative choices. At this point there is little information encoded, but unilateral inactivation of either the FOF or SC can easily push the network off the hill into one of the attractors, biasing the decision. Later, during the memory delay period, when the network resides in one of the attractors, there is a large amount of information encoded, but now the same perturbation is insufficient to push the network out of the attractor.
This network model makes two clear predictions which we test and confirm: 1) Simultaneous inactivation of the FOF and SC during the memory delay period should lead to a bias greater than the sum of inactivating either region alone; and 2) Inactivation during the cue presentation should bias difficult trials more than easy trials, but inactivation during the memory delay period should bias all trial types equally.
These results provide the first direct causal test that short-term memory is maintained by a network distributed across cortical and subcortical regions and is well characterized by attractor dynamics, but many questions still remain: What other brain area(s) are involved in this circuit? Do these findings generalize to short-term memory for other information? These any many other questions will continue to be the focus of future research.