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UCSD COGS 107B - Discharge Properties of Monkey Tectoreticular Neurons

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95:3502-3511, 2006. First published Apr 26, 2006; doi:10.1152/jn.00908.2005 J NeurophysiolC. Kip Rodgers, Douglas P. Munoz, Stephen H. Scott and Martin Paré Neurons Discharge Properties of Monkey Tectoreticular You might find this additional information useful...78 articles, 46 of which you can access free at: This article cites http://jn.physiology.org/cgi/content/full/95/6/3502#BIBLincluding high-resolution figures, can be found at: Updated information and services http://jn.physiology.org/cgi/content/full/95/6/3502 can be found at: Journal of Neurophysiologyabout Additional material and information http://www.the-aps.org/publications/jnThis information is current as of January 5, 2007 . http://www.the-aps.org/.American Physiological Society. ISSN: 0022-3077, ESSN: 1522-1598. Visit our website at (monthly) by the American Physiological Society, 9650 Rockville Pike, Bethesda MD 20814-3991. Copyright © 2005 by the publishes original articles on the function of the nervous system. It is published 12 times a yearJournal of Neurophysiology on January 5, 2007 jn.physiology.orgDownloaded fromDischarge Properties of Monkey Tectoreticular NeuronsC. Kip Rodgers,1,2Douglas P. Munoz,1,2,3Stephen H. Scott,1,4and Martin Pare´1,2,31Canadian Institutes of Health Research Group in Sensory-Motor Systems and Centre for Neuroscience Studies, and Departments of2Physiology3Psychology, and4Anatomy and Cell Biology, Queen’s University, Kingston, Ontario, CanadaSubmitted 31 August 2005; accepted in final form 20 March 2006Rodgers, C. Kip, Douglas P. Munoz, Stephen H. Scott, and MartinPare´. Discharge properties of monkey tectoreticular neurons. J Neu-rophysiol 95: 3502–3511, 2006; doi:10.1152/jn.00908.2005. The in-termediate layers of the superior colliculus (SC) contain neurons thatclearly play a major role in regulating the production of saccadic eyemovements: a burst of activity from saccade neurons (SNs) is thoughtto provide a drive signal to set the eyes in motion, whereas the tonicactivity of fixation neurons (FNs) is thought to suppress saccadesduring fixation. The exact contribution of these neurons to saccadecontrol is, however, unclear because the nature of the signals sent bythe SC to the brain stem saccade generation circuit has not beenstudied in detail. Here we tested the hypothesis that the SC outputsignal is sufficient to control saccades by examining whether anti-dromically identified tectoreticular neurons (TRNs: 33 SNs and 13FNs) determine the end of saccades. First, TRNs had dischargeproperties similar to those of nonidentified SC neurons and a propor-tion of output SNs had visually evoked responses, which signify thatthe saccade generator must receive and process visual information.Second, only a minority of TRNs possessed the temporal patterns ofactivity sufficient to terminate saccades: Output SNs did not ceasedischarging at the time of saccade end, possibly continuing to drivethe brain stem during postsaccadic fixations, and output FNs did notresume their activity before saccade end. These results argue againsta role for SC in regulating the timing of saccade termination by atemporal code and suggest that other saccade centers act to thwart theextraneous SC drive signal, unless it controls saccade termination bya spatial code.INTRODUCTIONNeurons in the intermediate layers of the primate superiorcolliculus (SC) have been shown to display activity necessaryfor regulating the production of saccadic eye movements (Pare´and Hanes 2003; Schiller et al. 1980; Sparks 1978). Consistentwith this role in saccade processing, many neurons in these SClayers are also known to send descending projections thatcontact neurons within the brain stem, including the parame-dian pontine reticular formation (PPRF), which innervate cra-nial nuclei to control extraocular muscles (Scudder et al. 2002;Sparks 2002). Nevertheless, the specific activity of monkeytectoreticular neurons (TRNs) has not been characterized inmore detail than to indicate that it is related to saccadeproduction (Gandhi and Keller 1997; Moschovakis et al. 1988;Scudder et al. 1996a). Little is therefore known about thedischarge properties of TRNs and whether they differ fromthose of unidentified SC neurons. The function of the SCbeyond movement initiation remains highly debated (Andersonet al. 1998; Goossens and van Opstal 2000; Munoz and Wurtz1995b; Port et al. 2000; Soetedjo et al. 2002; Waitman et al.1991) because it is unclear whether its neuronal activity con-trols saccade trajectory and/or specifies an updated eye dis-placement signal during saccades that can effectively signalsaccade termination. Here we studied the activity of antidromi-cally identified TRNs to determine the nature of the SCprojection to the brain stem saccade generator and whether itcarry signals appropriate to specify saccade termination.The intermediate layers of the SC contain two main popu-lations of neurons involved in saccade control. First, saccadeneurons (SNs) discharge a burst of activity that peaks aroundthe time of saccade onset, which is thought to provide a motorcommand specifying the vector of an upcoming saccade(Sparks 1978; Sparks and Mays 1980; Sparks et al. 1976). Thisburst of activity occurs during saccades to a limited region ofthe visual field known as the neuron’s movement field orresponse field (RF; for review, see Sparks 1986). These RFsare topographically organized and the SC forms a saccade map,with command signals for large saccades being coded in itscaudal portion and small saccades further rostrally (Ottes et al.1986; Robinson 1972). Second, fixation neurons (FNs), locatedin the very rostral SC, are tonically active when the eyes arestill and pause during saccades (Munoz and Guitton 1991;Munoz and Wurtz 1993a). This activity is thought to preventintrusive saccades (Munoz and Wurtz 1993b).We investigated the possible code in the SC output signalsthat could actively terminate saccades. Specifically, we testedtwo hypotheses by which the SC could temporally code the endof saccades by the activity of SNs and FNs. As first proposedby Waitzman et al. (1991), if the saccade burst from themajority of output SNs were highly attenuated (i.e., if they had“clipped” activity) at the time of saccade end, saccades couldbe terminated simply because of the absence of drive. In thisscenario, the activity of SNs is required to fall below a certainthreshold necessary to prolong a saccade. Accordingly, wewould expect to see not


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UCSD COGS 107B - Discharge Properties of Monkey Tectoreticular Neurons

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