Retrospective and prospective information coding by different neurons in the prefrontal cortex

Abstract

Neurons in the lateral prefrontal cortex exhibit sustained activity during the maintenance of visual memory. Previous studies also demonstrated that prefrontal neurons display predictive activity in anticipation of upcoming visual stimuli. Because these retrospective and prospective coding of visual stimuli have been examined in separate experiments, how these processes interact in individual neurons remains unknown. To examine this, we recorded from single prefrontal neurons while monkeys performed two behavioural tasks. In one task, the animals passively viewed a moving object during fixation, while in the other, they remembered the location of a briefly presented visual cue for subsequent saccades. We found that many neurons were reactive and responded only after the visual stimulus appeared in their receptive field, whereas some neurons were predictive and increased their activity even before the moving stimulus entered the receptive field. In the memory-guided saccade trials, the reactive neurons exhibited sustained activity during the delay period, whereas the predictive neurons did not. Delays of visual response to a moving stimulus did not correlate with visual latency for a stationary stimulus. Instead, it correlated with the magnitude of sustained activity during the delay period in the memory-guided saccade task. Our data show that retrospective and prospective coding of visual information are represented by distinct neuronal populations, and that their temporal preferences are stable across different task conditions. Reactive signals may reflect the amount of temporal integration in short-term memory, whereas predictive signals may solely represent future events in isolation from the maintenance of past information.

Temporal Dynamics of Hippocampal and Medial Prefrontal Cortex Interactions During the Delay Period of a Working Memory-Guided Foraging Task

“…These separate strategies appear to involve common neural circuits, including the PFC and HC in humans ( Mok 2012 ; Brown et al 2016 ) and rats ( Kesner 1989 ; Floresco et al 1997 ; Ferbinteanu and Shapiro 2003 ; Churchwell and Kesner 2011 ; Horst and Laubach 2012 ; Han et al 2013 ). Furthermore, neurophysiological data are consistent with both retrospective and prospective code in the 2 regions as the persistent delay-period activity in the rat and primate PFC contains information about previously presented stimuli as well as anticipated stimuli, goals, or actions ( Rainer et al 1999 ; Watanabe and Funahashi 2004 ; Luk and Wallis 2009 ; Horst and Laubach 2012 ; Hyman et al 2013 ; Matsushima and Tanaka 2013 ). Likewise, rat hippocampal place cells “replay” past maze locations ( Louie and Wilson 2001 ; Foster and Wilson 2006 ; Karlsson and Frank 2009 ) and fire in anticipation of future choice trajectories ( Ferbinteanu and Shapiro 2003 ; Itskov et al 2008 ; Pfeiffer and Foster 2013 ; Catanese et al 2014 ; Redish 2016 ).…”