Cortical and Subcortical Contributions to Short-Term Memory for Orienting Movements

• Published in: Neuron (Cambridge, Mass.) Vol. 88; no. 2; pp. 367 - 377
• Main Authors: Kopec, Charles D., Erlich, Jeffrey C., Brunton, Bingni W., Deisseroth, Karl, Brody, Carlos D.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 21.10.2015; Elsevier Limited
• Subjects: Acoustic Stimulation - methods; Animals; Behavior; Bias; Cerebral Cortex - physiology; Confidence intervals; Decision making; Derivatives; Experiments; Male; Memory, Short-Term - physiology; Monkeys & apes; Movement - physiology; Orientation - physiology; Rats; Rats, Long-Evans; Superior Colliculi - physiology; Transplants & implants
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/j.neuron.2015.08.033

Neural activity in frontal cortical areas has been causally linked to short-term memory (STM), but whether this activity is necessary for forming, maintaining, or reading out STM remains unclear. In rats performing a memory-guided orienting task, the frontal orienting fields in cortex (FOF) are considered critical for STM maintenance, and during each trial display a monotonically increasing neural encoding for STM. Here, we transiently inactivated either the FOF or the superior colliculus and found that the resulting impairments in memory-guided orienting performance followed a monotonically decreasing time course, surprisingly opposite to the neural encoding. A dynamical attractor model in which STM relies equally on cortical and subcortical regions reconciled the encoding and inactivation data. We confirmed key predictions of the model, including a time-dependent relationship between trial difficulty and perturbability, and substantial, supralinear, impairment following simultaneous inactivation of the FOF and superior colliculus during memory maintenance. •Optogenetics probes precisely when FOF and SC are needed for memory-guided orienting•Behavioral effect of silencing FOF or SC decreases monotonically during each trial•Attractor model reconciles decreasing perturbability with increasing neural encoding•Key attractor model predictions are confirmed Kopec et al. use transient optogenetic inactivation during memory-guided orienting to show that a simple attractor network model, distributed across cortex and the superior colliculus, can account for both monotonically increasing neural encoding and monotonically decreasing behavioral effects of inactivation.