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

Abstract

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 timecourse, 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.

Mechanisms of Persistent Activity in Cortical Circuits: Possible Neural Substrates for Working Memory

“…To causally test the role of delay period activity in WM, recent work has focused on single-trial analyses of neural activity and behavior and on the impact of optogenetic perturbations on the behavioral reports at the end of the delay period; as argued by Panzeri et al (2017), these two techniques provide powerful tests of the causal role of neural activities in driving behavior. This work shows that, even over trials in which the animal had to remember the same presented stimulus, differences in the delay period activities are predictive of subsequent differences in the behavior (Kopec et al 2015, Li et al 2016, Vergara et al 2016, Wimmer et al 2014). Moreover, optogenetic perturbations to the neural activities during the delay period cause predictable changes in the subsequent behavior (Kopec et al 2015, Li et al 2016, Liu et al 2014).…”

“…Recent work has expanded to rodents, in which genetic tools allow neural activities to be manipulated as well as recorded. That work has focused on rodent homologs of the primate brain areas involved in memory and movement planning, including the parietal cortex, PFC, anterior lateral motor cortex (ALM), frontal orienting fields (FOF), and superior colliculus (SC) (Harvey et al 2012, Kopec et al 2015, Li et al 2016, Liu et al 2014). In rodents, elevated delay period firing is observed as in the monkey, but relatively few cells are active for the entire delay period.…”

Robust neuronal dynamics in premotor cortex during motor planning

“…After ipsilateral photoinhibition ALM activity rapidly recovered to the unperturbed trajectory (Figs 1, 3). This is inconsistent with attractors with a pair of fixed points (one for each choice condition) 29 . Upon release from perturbation these models decay to the final fixed point and do not return to the trajectory (Extended Data Fig.…”

Segregated fronto‐cortical and midbrain connections in the mouse and their relation to approach and avoidance orienting behaviors

“…Lesions of M2 in rats cause a deficit in orienting, while microstimulation elicits orienting type behaviors (Cowey & Bozek, 1974; Sinnamon & Galer, 1984). A recent study has indicated that both the M2 and the SCl are involved in the generation of short term memory representations that are required for sensory orienting (Kopec, Erlich, Brunton, Deisseroth, & Brody, 2015). Taken together this information lends weight to the role of the M2 area in guiding orienting approach related behaviors which are mediated via the SCl.…”