Abstract
A central goal of cognitive neuroscience is to elucidate the neural mechanisms underlying decision-making. Recent physiological studies suggest that neurons in association areas may be involved in this process. To test this, we measured the effects of electrical microstimulation in the lateral intraparietal area (LIP) while monkeys performed a reaction-time motion discrimination task with a saccadic response. In each experiment, we identified a cluster of LIP cells with overlapping response fields (RFs) and sustained activity during memory-guided saccades. Microstimulation of this cluster caused an increase in the proportion of choices toward the RF of the stimulated neurons. Choices toward the stimulated RF were faster with microstimulation, while choices in the opposite direction were slower. Microstimulation never directly evoked saccades, nor did it change reaction times in a simple saccade task. These results demonstrate that the discharge of LIP neurons is causally related to decision formation in the discrimination task.
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References
de Lafuente, V. & Romo, R. Neuronal correlates of subjective sensory experience. Nat. Neurosci. 8, 1698–1703 (2005).
Schall, J. & Thompson, K. Neural selection and control of visually guided eye movements. Annu. Rev. Neurosci. 22, 241–259 (1999).
Glimcher, P.W. The neurobiology of visual-saccadic decision making. Annu. Rev. Neurosci. 26, 133–179 (2003).
Romo, R. & Salinas, E. Flutter discrimination: neural codes, perception, memory and decision making. Nat. Rev. Neurosci. 4, 203–218 (2003).
Pasternak, T. & Merigan, W.H. Motion perception following lesions of the superior temporal sulcus in the monkey. Cereb. Cortex 4, 247–259 (1994).
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. The analysis of visual motion: a comparison of neuronal and psychophysical performance. J. Neurosci. 12, 4745–4765 (1992).
Salzman, C.D., Murasugi, C.M., Britten, K.H. & Newsome, W.T. Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci. 12, 2331–2355 (1992).
Newsome, W.T. & Paré, E.B. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J. Neurosci. 8, 2201–2211 (1988).
Gold, J.I. & Shadlen, M.N. The influence of behavioral context on the representation of a perceptual decision in developing oculomotor commands. J. Neurosci. 23, 632–651 (2003).
Roitman, J.D. & Shadlen, M.N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 22, 9475–9489 (2002).
Shadlen, M.N. & Newsome, W.T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 86, 1916–1936 (2001).
Colby, C.L. & Goldberg, M.E. Space and attention in parietal cortex. Annu. Rev. Neurosci. 22, 319–349 (1999).
Andersen, R.A. & Buneo, C.A. Intentional maps in posterior parietal cortex. Annu. Rev. Neurosci. 25, 189–220 (2002).
Born, R.T. & Bradley, D.C. Structure and function of visual area MT. Annu. Rev. Neurosci. 28, 157–189 (2005).
Britten, K.H., Shadlen, M.N., Newsome, W.T. & Movshon, J.A. Responses of neurons in macaque MT to stochastic motion signals. Vis. Neurosci. 10, 1157–1169 (1993).
Ditterich, J., Mazurek, M. & Shadlen, M.N. Microstimulation of visual cortex affects the speed of perceptual decisions. Nat. Neurosci. 6, 891–898 (2003).
Ratcliff, R. & Rouder, J.N. Modeling response times for two-choice decisions. Psychol. Sci. 9, 347–356 (1998).
Mazurek, M.E., Roitman, J.D., Ditterich, J. & Shadlen, M.N. A role for neural integrators in perceptual decision making. Cereb. Cortex 13, 1257–1269 (2003).
Holmes, P. et al. Optimal decisions: from neural spikes, through stochastic differential equations, to behavior. IEICE Transactions on Fundamentals of Electronics, Communications and Computer Science 88, 2496–2503 (2005).
Ratcliff, R. & Smith, P. A comparison of sequential sampling models for two-choice reaction time. Psychol. Rev. 111, 333–367 (2004).
Link, S.W. The Wave Theory of Difference and Similarity (Lawrence Erlbaum Associates, Hillsdale, New Jersey, 1992).
Palmer, J., Huk, A.C. & Shadlen, M.N. The effect of stimulus strength on the speed and accuracy of a perceptual decision. J. Vis. 5, 376–404 (2005).
Bisley, J.W., Zaksas, D. & Pasternak, T. Microstimulation of cortical area MT affects performance on a visual working memory task. J. Neurophysiol. 85, 187–196 (2001).
Gottlieb, J. & Goldberg, M.E. Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task. Nat. Neurosci. 2, 906–912 (1999).
Wardak, C., Olivier, E. & Duhamel, J.R. A deficit in covert attention after parietal cortex inactivation in the monkey. Neuron 42, 501–508 (2004).
Bisley, J.W. & Goldberg, M.E. Neuronal activity in the lateral intraparietal area and spatial attention. Science 299, 81–86 (2003).
Gottlieb, J.P., Kusunoki, M. & Goldberg, M.E. The representation of visual salience in monkey parietal cortex. Nature 391, 481–484 (1998).
Platt, M.L. & Glimcher, P.W. Responses of intraparietal neurons to saccadic targets and visual distractors. J. Neurophysiol. 78, 1574–1589 (1997).
Pare, M. & Wurtz, R.H. Progression in neuronal processing for saccadic eye movements from parietal cortex area lip to superior colliculus. J. Neurophysiol. 85, 2545–2562 (2001).
Gold, J.I. & Shadlen, M.N. Neural computations that underlie decisions about sensory stimuli. Trends Cogn. Sci. 5, 10–16 (2001).
Schiller, P.H. & Tehovnik, E.J. Look and see: how the brain moves your eyes about. Prog. Brain Res. 134, 127–142 (2001).
Burman, D.D. & Bruce, C.J. Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. J. Neurophysiol. 77, 2252–2267 (1997).
Opris, I., Barborica, A. & Ferrera, V.P. Effects of electrical microstimulation in monkey frontal eye field on saccades to remembered targets. Vision Res. 45, 3414–3429 (2005).
Romo, R., Hernandez, A. & Zainos, A. Neuronal correlates of a perceptual decision in ventral premotor cortex. Neuron 41, 165–173 (2004).
Kim, J.-N. & Shadlen, M.N. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat. Neurosci. 2, 176–185 (1999).
Horwitz, G.D. & Newsome, W.T. Target selection for saccadic eye movements: prelude activity in the superior colliculus during a direction-discrimination task. J. Neurophysiol. 86, 2543–2558 (2001).
Huk, A.C. & Shadlen, M.N. Neural activity in macaque parietal cortex reflects temporal integration of visual motion signals during perceptual decision making. J. Neurosci. 25, 10420–10436 (2005).
Carello, C.D. & Krauzlis, R.J. Manipulating intent: evidence for a causal role of the superior colliculus in target selection. Neuron 43, 575–583 (2004).
Eskandar, E.N. & Assad, J.A. Dissociation of visual, motor and predictive signals in parietal cortex during visual guidance. Nat. Neurosci. 2, 88–93 (1999).
Leon, M.I. & Shadlen, M.N. Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38, 317–327 (2003).
Sugrue, L.P., Corrado, G.S. & Newsome, W.T. Matching behavior and the representation of value in the parietal cortex. Science 304, 1782–1787 (2004).
Platt, M.L. & Glimcher, P.W. Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999).
Brainard, D.H. The psychophysics toolbox. Spat. Vis. 10, 443–446 (1997).
Lewis, J.W. & Van Essen, D.C. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J. Comp. Neurol. 428, 112–137 (2000).
Van Essen, D.C. et al. An integrated software suite for surface-based analyses of cerebral cortex. J. Am. Med. Inform. Assoc. 8, 443–459 (2001).
Tehovnik, E.J. Electrical stimulation of neural tissue to evoke behavioral responses. J. Neurosci. Methods 65, 1–17 (1996).
Butovas, S. & Schwarz, C. Spatiotemporal effects of microstimulation in rat neocortex: a parametric study using multielectrode recordings. J. Neurophysiol. 90, 3024–3039 (2003).
Thier, P. & Andersen, R.A. Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. J. Neurophysiol. 80, 1713–1735 (1998).
Smith, P. A note on the distribution of response times for a random walk with gaussian increments. J. Math. Psychol. 34, 445–459 (1990).
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. Numerical Recipes in C 735 (Cambridge University Press, Cambridge, UK, 1988).
Acknowledgements
We thank A. Huk, M. Mazurek and W. Newsome for helpful discussion on all aspects of this project; S. Allred, A. Churchland, R. Kiani, J. Palmer and T. Yang for comments on this manuscript and useful suggestions; and M. Mihali, J. McNulty and V.K. Skypeck for technical assistance. This study was supported by the Howard Hughes Medical Institute (HHMI) and the National Eye Institute. T.D.H. is also supported by an HHMI predoctoral fellowship.
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Hanks, T., Ditterich, J. & Shadlen, M. Microstimulation of macaque area LIP affects decision-making in a motion discrimination task. Nat Neurosci 9, 682–689 (2006). https://doi.org/10.1038/nn1683
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DOI: https://doi.org/10.1038/nn1683
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