Microsaccades as a marker not a cause for attention-related modulation

Abstract

Recent evidence suggests that microsaccades are causally linked to the attention-related modulation of neurons—specifically, that microsaccades toward the attended location are required for the subsequent changes in firing rate. These findings have raised questions about whether attention-related modulation is due to different states of attention as traditionally assumed or might instead be a secondary effect of microsaccades. Here, in two rhesus macaques, we tested the relationship between microsaccades and attention-related modulation in the superior colliculus (SC), a brain structure crucial for allocating attention. We found that attention-related modulation emerged even in the absence of microsaccades, was already present prior to microsaccades toward the cued stimulus, and persisted through the suppression of activity that accompanied all microsaccades. Nonetheless, consistent with previous findings, we also found significant attention-related modulation when microsaccades were directed toward, rather than away from, the cued location. Thus, despite the clear links between microsaccades and attention, microsaccades are not necessary for attention-related modulation, at least not in the SC. They do, however, provide an additional marker for the state of attention, especially at times when attention is shifting from one location to another.

Functional but not obligatory link between microsaccades and neural modulation by covert spatial attention

“…This directional biasing of microsaccades, however, will only occur when activity in the oculomotor system reaches the threshold for outputting a microsaccade. At times at which activity in the oculomotor system is not close to outputting a saccade, the same oculomotor system may nonetheless contribute to shifting attention without concomitantly yielding an overt reflection in the form of a microsaccade 8 , 41 , 42 . Thus, directionally biased microsaccades and neural modulation may reflect two separate manifestations of covert selective attention operations that may each be mediated (at least in part) by the same oculomotor circuitry.…”

“…When crossing the threshold for an overt microsaccade, the timing and direction of microsaccades functionally co-vary with the timing and direction of EEG-alpha modulation (and other neural signatures such as spike-rate; as in refs. 21 , 42 ). Future work targeting neural activity in and outside the oculomotor system in trials with and without microsaccades is required to substantiate this threshold interpretation.…”

“… 43 , 44 ) neural modulation by covert attention to occur (see also ref. 42 ). Just like our data reveal how neural modulation by covert attention may occur without concurrent microsaccades, complementary studies have suggested that not all microsaccades are necessarily associated with shifts of attention 44 , 45 .…”

Internal selective attention is delayed by competition between endogenous and exogenous factors

“…However, as the authors of this study acknowledged, this hypothesis cannot be substantiated based on microsaccades alone. First, although attention-related modulations of cortical and subcortical processing are larger during trials containing microsaccades towards the location of a (covertly) attended stimulus, clear attention-related modulations are also observed in the absence of microsaccades (Yu et al, 2022; Liu et al, 2022; though see Lowet et al 2018 for a contradictory result). Second, any of the three models examined in the current study (i.e., retro-capture, automatic refreshing, or delayed selection) could have produced the delays in microsaccade biases reported by van Ede et al (2020).…”

All eyes on attention

“…Now, in eLife, Gongchen Yu, Richard Krauzlis and colleagues at the National Eye Institute, Bethesda and the University of Pittsburgh report cleverly designed experiments that help to address this crucial question ( Yu et al, 2022 ). In particular, they managed to disentangle confounding factors which limited previous investigations into this topic ( Meyberg et al, 2017 ).…”