Short‐duration stimulation of the supplementary eye fields perturbs anti‐saccade performance while potentiating contralateral head orienting

Abstract

Many forms of brain stimulation utilize the notion of state dependency, whereby greater influences are observed when a given area is more engaged at the time of stimulation. Here, by delivering intracortical microstimulation (ICMS) to the supplementary eye fields (SEF) of monkeys performing interleaved pro- and anti-saccades, we show a surprising diversity of state-dependent effects of ICMS-SEF. Short-duration ICMS-SEF passed around cue presentation selectively disrupted anti-saccades by increasing reaction times and error rates bilaterally, and also recruited neck muscles, favoring contralateral head turning to a greater degree on anti-saccade trials. These results are consistent with the functional relevance of the SEF for anti-saccades. The multiplicity of stimulation-evoked effects, with ICMS-SEF simultaneously disrupting anti-saccade performance and facilitating contralateral head orienting, probably reflects both the diversity of cortical and subcortical targets of SEF projections, and the response of this oculomotor network to stimulation. We speculate that the bilateral disruption of anti-saccades arises via feedback loops that may include the thalamus, whereas neck muscle recruitment arises via feedforward polysynaptic pathways to the motor periphery. Consideration of both sets of results reveals a more complete picture of the highly complex and multiphasic response to ICMS-SEF that can play out differently in different effector systems.

Evidence for a functional subdivision of Premotor Ear-Eye Field (Area 8B)

“…Similar results were found by Mitz and Godschalk ( 1989 ) when stimulating a region corresponding to the PEEF. Moreover, this phenomenon is in accord with Chapman and Corneil ( 2014 ), who found that short ICMS of SEF did not evoke saccades during the task performance, even if it influenced the percentage of errors and the reaction times of the anti-saccades and pro-saccades.…”

“…Because the monkeys fixated spontaneously on regions of the space—which then meant that we needed to repeat the stimulation several times while the monkeys gazed in a variety of directions—it is reasonable to expect to find higher latencies in PEEF in comparison to other similar studies. For example, stimulation of the SEF elicited eye movements having latencies ranging from 40 to 160 ms (Chapman et al, 2012 ) and from 60 to 120 ms (Chapman and Corneil, 2014 ). Yang et al ( 2008 ) found when stimulating the dorsomedial frontal cortex (DMFC) that the latency of the evoked movements was about 80–86 ms, accompanied by a small standard deviation, even though they found also that the latency change was not correlated with the change in endpoint and saccade metrics or dynamics.…”

“…Other brain regions have been shown to have a role in gaze shift, with particular reference to the FEF (Bizzi and Schiller, 1970 ; Azuma and Suzuki, 1984 ; Bruce and Goldberg, 1985 ; Bruce et al, 1985 ; Azuma et al, 1988 ; Blanke et al, 1999 ; Chen, 2006 ; Elsley et al, 2007 ; Knight and Fuchs, 2007 ; Monteon et al, 2010 , 2013 ; Knight, 2012 ; Funahashi, 2014 ), SEF (Bon and Lucchetti, 1992 ; Chen and Wise, 1995a , b , 1997 ; Amador et al, 2004 ; Chen and Walton, 2005 ; Chapman et al, 2012 ; Chapman and Corneil, 2014 ) and superior colliculus (Stryker and Schiller, 1975 ; Stein and Clamann, 1981 ; Stanford et al, 1996 ; Freedman and Sparks, 1997 ; Corneil et al, 2002 ; Populin et al, 2004 ). In support, superior colliculus hosts neurons integrating visual and auditory information (Stein and Stanford, 2008 ) and its stimulation in cats revealed the presence of an ear motor map overlapping with an eye motor map (Stein and Clamann, 1981 ).…”

LATER models of neural decision behavior in choice tasks

“…Such an idea is not itself a new one, for example there is some evidence that the supplementary eye field monitors the results of decision processes regarding eye movements (Carpenter, 2004) and this area is thought to be important in anti-saccades (Chapman and Corneil, 2014). …”

Neuronal Encoding of Self and Others’ Head Rotation in the Macaque Dorsal Prefrontal Cortex

“…Indeed, we identified two main anatomo-functional cortical networks. The first is a dorso/mesial network, encompassing head/gaze-related brain regions such as the dorsal part of FEF 33 , 34 , SEF 8 , 12 , 70 , PEEF 30 , and the parietal, retrosplenial, and entorhinal cortex 38 , 41 . This network may be involved in the transformation of sensory signals into head motor commands in order to drive shifts of attention and rotate the head toward a specific spatial region.…”