The puzzle of spontaneous alternation and inhibition of return: How they might fit together

Abstract

Two isolated spatial phenomena share a similar “been there; done that” effect on spatial behavior. Originally discovered in rodent learning experiments, spontaneous alternation is a tendency for the organism to visit a different arm in a T‐maze on subsequent trials. Originally discovered in human studies of attention, inhibition of return is a tendency for the organism to orient away from a previously attended location. Whereas spontaneous alternation was identified by O'Keefe & Nadel as dependent on an intact hippocampus, inhibition of return is dependent on neural structures that participate in oculomotor control (the superior colliculus, parietal and frontal cortex). Despite the isolated literatures, each phenomenon has been assumed to reflect a basic novelty‐seeking process, avoiding places previously visited or locations attended. In this commentary, we explore and compare the behavioral manifestations and neural underpinnings of these two phenomena, and suggest what is still needed to determine whether they operate in parallel or serial.

Intracranial Recordings Demonstrate Both Cortical and Medial Temporal Lobe Engagement in Visual Search in Humans

“…Our results instead suggest that the MTL is selectively engaged during the on-line search behavior. This is consistent with several accounts of putative MTL engagement in search, including: 1) eye movement studies suggesting that the on-line search process requires memory (Peterson et al, 2001(Peterson et al, , 2008McCarley et al, 2003); 2) elicitation of MTL engagement by novel stimuli, as required by pop-out (Parker et al, 1998;Knight, 1996;von Restorff, 1933); 3) hypothesized MTL engagement in IOR as a visual foraging behavior (Phillmore & Klein, 2019); 4) a role for the MTL in detection of familiar stimuli (match enhancement; Dudukovic, Preston, Archie, Glover, & Wagner, 2011); 5) a role for the hippocampus in relational processing of images (Córdova, Turk-Browne, & Aly, 2019); and 6) a navigation account of visual search whereby a geometric map of the visual search display is formed in the entorhinal grid cell system (Nau et al, 2018;Meister & Buffalo, 2016). These accounts are not mutually exclusive, and it is possible that future theoretical work will bring them together into a unified theory.…”

“…On a shorter temporal scale, the phenomenon of inhibition of return (IOR), a process that facilitates visual exploration of novel objects by inhibiting revisits to previously attended objects (Posner, Rafal, Choate, & Vaughan, 1985), can be viewed as a subprocess of visual search related to novelty. Phillmore and Klein (2019) recently outlined parallels between IOR and spontaneous alternation in rodents (Tolman, 1925), noting that both are noveltyseeking spatial foraging behaviors. Because hippocampal lesions impair spontaneous alternation, Phillmore and Klein (2019) propose that future work should examine whether IOR, a visual exploration behavior, is also impaired by MTL lesions.…”

“…Phillmore and Klein (2019) recently outlined parallels between IOR and spontaneous alternation in rodents (Tolman, 1925), noting that both are noveltyseeking spatial foraging behaviors. Because hippocampal lesions impair spontaneous alternation, Phillmore and Klein (2019) propose that future work should examine whether IOR, a visual exploration behavior, is also impaired by MTL lesions.…”

The intersection between the oculomotor and hippocampal memory systems: empirical developments and clinical implications

“…Neurally, these retention signals have been considered to be restricted to either the frontoparietal network or subcortical control areas . It remains an open question whether the memory signals attributed to IOR or VWM are supported by functions of the hippocampus; recent writings have called for further inquiry . Regardless, traditional models of oculomotor control have not accounted for the broader collection of findings that point to a role for memory representations mediated by the hippocampus and MTL in the guidance of eye movements.…”

“…[68][69][70] It remains an open question whether the memory signals attributed to IOR or VWM are supported by functions of the hippocampus; recent writings have called for further inquiry. 71,72 Regardless, traditional models of oculomotor control have not accounted for the broader collection of findings that point to a role for memory representations mediated by the hippocampus and MTL in the guidance of eye movements. Specifically, whereas individuals may not necessarily need to rely on the functions of the hippocampus and MTL to guide viewing in accordance with long-established semantic memories (as in the work of Yarbus 3 and Loftus and Mackworth 4 ), viewing behavior that changes in accordance with recent experience 5 or that emerges in response to a task that has high relational memory demands (including perceptual processing or visual search tasks 27,73 ) would seem to require the contributions of the hippocampus and MTL.…”