Top-down signal from prefrontal cortex in executive control of memory retrieval

Abstract

Knowledge or experience is voluntarily recalled from memory by reactivation of the neural representations in the cerebral association cortex. In inferior temporal cortex, which serves as the storehouse of visual long-term memory, activation of mnemonic engrams through electric stimulation results in imagery recall in humans, and neurons can be dynamically activated by the necessity for memory recall in monkeys. Neuropsychological studies and previous split-brain experiments predicted that prefrontal cortex exerts executive control upon inferior temporal cortex in memory retrieval; however, no neuronal correlate of this process has ever been detected. Here we show evidence of the top-down signal from prefrontal cortex. In the absence of bottom-up visual inputs, single inferior temporal neurons were activated by the top-down signal, which conveyed information on semantic categorization imposed by visual stimulus-stimulus association. Behavioural performance was severely impaired with loss of the top-down signal. Control experiments confirmed that the signal was transmitted not through a subcortical but through a fronto-temporal cortical pathway. Thus, feedback projections from prefrontal cortex to the posterior association cortex appear to serve the executive control of voluntary recall.

Top-down facilitation of visual recognition

“…Indeed, event-related potentials studies (56,57) have repeatedly shown that humans can distinguish between the category of objects in scenes extremely rapidly, which we argue can be mediated by coarse LSF representations, and that this distinction is first apparent in prefrontal cortex time courses Ϸ150 ms from stimulus onset. That such prefrontal representations subsequently guide the activation of IT representations is supported by fMRI studies in human patients (9,58) and electrophysiology recordings in monkeys (10).…”

“…This view has been challenged by models proposing a simultaneous bottom-up and top-down flow of information in the cortex (1)(2)(3)(4)(5)(6). Recent findings support those proposals by showing that top-down mechanisms might play an important role in visual processing (7)(8)(9)(10), but it remains puzzling how such processing would be initiated. Indeed, the existence of top-down processes that facilitate perception implies that high-level information is activated earlier than some lower-level information.…”

Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations

“…Neurons in the PFC receive highly processed information to represent abstract categories 46,47 irrespective of sensory modality 48 . The PFC actively retrieves associative representations from long-term memory for top-down control 49 and establishes semantic associations between arbitrary items and meaningful categories 50,51 . However, such abstract representations and semantic associations also need to be processed according to rules and strategies to produce situational and strategic communicative utterances.…”

Early onset of neural synchronization in the contextual associations network

“…Generally, neural activity after about 200-300 ms has been associated predominantly with feedback processes (57,58). Therefore, this relatively late phase locking between the RSC and occipital cortex may reflect feedback from the RSC to early visual areas.…”