A Neural Mechanism for Microsaccade Generation in the Primate Superior Colliculus

Abstract

During fixation, the eyes are not still, but often exhibit microsaccadic movements. The function of microsaccades is controversial, largely because the neural mechanisms responsible for their generation are unknown. Here we show that the superior colliculus (SC), a retinotopically organized structure involved in voluntary-saccade target selection, plays a causal role in microsaccade generation. Neurons in the foveal portion of the SC increase their activity before and during microsaccades with sizes of only a few minutes of arc, and exhibit selectivity for the direction and amplitude of these movements. Reversible inactivation of these neurons significantly reduces microsaccade rate without otherwise compromising fixation. These results, coupled with computational modeling of SC activity, demonstrate that microsaccades are controlled by the SC, and explain the link between microsaccades and visual attention.Microsaccades are the very small (typically <12 min arc), involuntary, fast eye movements that occur during fixation (1-3). The behavioral properties and functional significance of microsaccades have been extensively studied -and sometimes vigorously debated -for many years (1-14). However, the neural mechanisms responsible for their generation are unexplored. We now show that the superior colliculus (SC), a retinotopically organized structure known to be important for selecting and initiating voluntary eye movements (15)(16)(17), is also part of the neural mechanism that controls microsaccades.We analyzed SC activity associated with 15,205 microsaccades that occurred while monkeys fixated a small stationary spot (18). Each fixation trial lasted for 3,500 ms resulting in many microsaccades with a variety of directions and amplitudes (Fig. 1A,Supp. Fig. S1). These movements had dynamics like those of larger saccades (3) (Supp. Fig. S1A), consistent with evidence that pre-motor neurons (downstream from the SC) are active during movements as small as 12-15 min arc (19).We targeted neurons in the rostral pole of the SC, which represents foveal goal locations (18,20). Figure 1A shows the spiking activity of a neuron in the left SC during a single trial containing 9 microsaccades (highlighted in green). The neuron exhibited changes in activity that were correlated with microsaccades. For example, the microsaccades labeled 1 and 2 in Fig. 1A were predominantly downward and leftward, respectively, and both were associated with a reduction in the neuron's activity. In contrast, small, predominantly rightward † This manuscript has been accepted for publication in Science. This version has not undergone final editing. Please refer to the complete version of record at http://www.sciencemag.org/. The manuscript may not be reproduced or used in any manner that does not fall within the fair use provisions of the Copyright Act without the prior, written permission of AAAS.*To whom correspondence should be addressed. E-mail: zhafed@salk.edu. NIH Public Access Author ManuscriptScience. Author manuscript; available in P...

Microsaccade Control Signals in the Cerebellum

“…This is larger than in most studies, although there is also considerable variability between the average microsaccade amplitudes described in past reports, which include 0.8° (Bair and O'Keefe, 1998) (Ko et al, 2010;Poletti and Rucci, 2010), and 0.23° ( Hafed et al, 2009).…”

“…Moreover, the activity of microsaccade-selective neurons during macrosaccades was similar to the activity of macrosaccade-selective neurons during microsaccades, indicating a continuous representation of amplitude in the cerebellum. These results dovetail nicely with recent work showing that muscimol injection to the fastigial oculomotor region, the output structure of the oculomotor vermis (Yamada and Noda, 1987;Noda et al, 1990), biases the endpoints of both microsaccades and macrosaccades to ipsilesional space (Goffart et al, 2004;Guerrasio et al, 2010) and a growing body of research suggesting that the functions of the oculomotor control system are similar for microsaccades and macrosaccades (Van Gisbergen et al, 1981;Brien et al, 2009;Hafed et al, 2009;Ko et al, 2010;Hafed, 2011;Hafed and Krauzlis, 2012;Van Horn and Cullen, 2012;Poletti et al, 2013). We conclude that the cerebellum's role in the control of saccades extends even to the oculomotor system's smallest saccades, which occur during fixation.…”

“…It has been shown that recently this collicular zone also triggers microsaccades (Hafed et al, 2009;Hafed and Krauzlis, 2012). Saccade amplitude is represented along the caudal-rostral axis, with macrosaccades represented in the caudal sector and microsaccades represented in the rostral pole of the superior colliculus.…”

An oculomotor continuum from exploration to fixation

“…No studies to date have conducted recordings from inhibitory burst neurons in connection with microsaccades, however (31). Omnipause neurons in the raphe stop firing during both saccades and microsaccades (32,33), and population activity in the superior colliculus map generates microsaccades and saccades in equivalent fashion (9,34). The hypothesis of a fixation-exploration continuum reconciles the dynamics of oculomotor behavior with the proposal of a common microsaccade-saccade generator (9-11), and it moreover elucidates previously unexplained results concerning the precise relationship between saccades and microsaccades, such as the finding that subjects can make voluntary saccades that are as small as fixational microsaccades (12).…”

Endogenous Attention Signals Evoked by Threshold Contrast Detection in Human Superior Colliculus

“…Additionally, the task may have modulated subjects' fixational eye movements. SC contains neurons responsive to microsaccades near the foveal (rostral) regions (Hafed et al, 2009), and recent evidence has suggested a link between microsaccades and covert attention (Engbert and Kliegl, 2003;Hafed et al, 2009). However, in our experiment the observed responses were in more central regions of SC that correspond to the peripheral visual field, reducing the likelihood that the responses were generated by microsaccade-related activity.…”