Requirement of Prefrontal and Midbrain Regions for Rapid Executive Control of Behavior in the Rat

Abstract

To study rapid sensorimotor remapping, we developed a method to train rats in a behavior in which subjects are cued, on each trial, to apply a sensorimotor association to orient either toward a visual target ("Pro") or away from it, toward its reverse ("Anti"). Multiple behavioral asymmetries suggested that Anti behavior is cognitively demanding while Pro is easier to learn and perform. This is consistent with a prominent hypothesis in the primate literature that Anti requires prefrontal cortex (PFC), whereas Pro could be mediated by midbrain superior colliculus (SC). Pharmacological inactivation of rat medial PFC supported its expected role in Anti. Remarkably, bilateral SC inactivation substantially impaired Anti while leaving Pro essentially intact. Moreover, SC inactivation eliminated the performance cost of switching from Anti to Pro tasks. Our results establish a rodent model of single-trial sensorimotor remapping and suggest a critical role for SC in the cognitively demanding Anti task.

Fast and slow transitions in frontal ensemble activity during flexible sensorimotor behavior

“…A key difference is that prior studies have focused on the learning of novel sensorimotor mappings or new rules, whereas our task requires animals to repeatedly disengage and re-engage the learned associations required for sound-guided trials. Likewise, although our paradigm shares important features with other assays for flexibility 7,9,10,12,39–41 , there are also crucial differences (see Methods).…”

Discrete Circuits Support Generalized versus Context-Specific Vocal Learning in the Songbird

“…In contrast, when context-specificity is appropriate - for example, to modify central commands in a manner that accounts for context-dependent dynamics of the musculoskeletal system (Bouchard and Chang, 2014; Ostry et al, 1996; Schmidt and Wild, 2014; Wohlgemuth et al, 2010) - conflicting biasing signals will interfere with consolidation, and learning will continue to rely on moment-by-moment modulation by the AFP. Such a dependence of consolidation on the coherence of AFP bias may therefore be a natural way for the nervous system to transfer modifications that are generally appropriate to primary motor circuitry, while reserving frontal, “executive” circuitry for dynamically adjusting performance in response to context-specific requirements (Duan et al, 2015; Hilario et al, 2012; Kim and Hikosaka, 2013; Miller and Cohen, 2001; Narayanan and Laubach, 2006). …”

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

“…In rats, appetitive hunting and whisking behavior results in increased c‐FOS expression within the SCl, and lesions of the SCl decrease predatory orienting behaviors (Favaro et al, 2011; Furigo et al, 2010). Research groups who investigate auditory or odor cued orienting responses in the SC often place probes (electrodes, optrodes) in the lateral portion of the SC (Duan, Erlich, & Brody, 2015; Felsen & Mainen, 2012; Stubblefield, Costabile, & Felsen, 2013), and thus our knowledge regarding stimulus processing in the mouse SC might be biased toward appetitive stimulus types. Once processed, the SCl sends the information through the crossed tecto‐reticulo‐spinal tract to brain stem motor nuclei to initiate approach behavior (Redgrave, Dean, & Westby, 1990).…”