Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T05:40:59.211Z Has data issue: false hasContentIssue false
  • English
  • Français

Linking neural activity to complex decisions

Published online by Cambridge University Press:  16 September 2013

BENJAMIN HAYDEN  and
TATIANA PASTERNAK
BENJAMIN HAYDEN*
Affiliation:
Brain and Cognitive Sciences, Center for Visual Science, University of Rochester, Rochester, New York
TATIANA PASTERNAK
Affiliation:
Brain and Cognitive Sciences, Center for Visual Science, University of Rochester, Rochester, New York Department of Neurobiology and Anatomy, University of Rochester Medical Center, Center for Visual Science, University of Rochester, Rochester, New York
*
*Address correspondence to: Dr. Benjamin Hayden, University of Rochester, Brain and Cognitive Sciences, Center for Visual Science, University of Rochester, Rochester, NY 14621. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

In the 1990s, seminal work from Newsome and colleagues made it possible to study the neuronal mechanisms of simple perceptual decisions. The key strength of this work was the clear and direct link between neuronal activity and choice processes. Since then, a great deal of research has extended these initial discoveries to more complex forms of decision making, with the goal of bringing the same strength of linkage between neural and psychological processes. Here, we discuss the progress of two such research programs, namely our own, that are aimed at understanding memory-guided decisions and reward-guided decisions. These problems differ in the relevant brain areas, in the progress that has been achieved, and in the extent of broader understanding achieved so far. However, they are unified by the use of theoretical insights about how to link neuronal activity to decisions.

Keywords

Working memoryDecision makingChoice probabilityRewardPrefrontal cortex
Type
Linking performance and neural mechanisms in adults
Information
Visual Neuroscience , Volume 30 , Special Issue 5-6: Linking Hypotheses in Visual Neuroscience: A Tribute to Davida Teller , November 2013 , pp. 331 - 342
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Afraz, S.R., Kiani, R. & Esteky, H. (2006). Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692–695.CrossRefGoogle ScholarPubMed
Amiez, C., Joseph, J.P. & Procyk, E. (2006). Reward encoding in the monkey anterior cingulate cortex. Cerebral Cortex 16, 1040–1055.CrossRefGoogle ScholarPubMed
Averbeck, B.B., Sohn, J.W. & Lee, D. (2006). Activity in prefrontal cortex during dynamic selection of action sequences. Nature Neuroscience 9, 276–282.CrossRefGoogle ScholarPubMed
Balleine, B.W., Delgado, M.R. & Hikosaka, O. (2007). The role of the dorsal striatum in reward and decision-making. The Journal of Neuroscience 27, 8161–8165.CrossRefGoogle ScholarPubMed
Barbas, H. (1988). Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. The Journal of Comparative Neurology 276, 313–342.CrossRefGoogle ScholarPubMed
Barraclough, D.J., Conroy, M.L. & Lee, D. (2004). Prefrontal cortex and decision making in a mixed-strategy game. Nature Neuroscience 7, 404–410.CrossRefGoogle Scholar
Bendiksby, M.S. & Platt, M.L. (2006). Neural correlates of reward and attention in macaque area LIP. Neuropsychologia 44, 2411–2420.CrossRefGoogle ScholarPubMed
Bernacchia, A., Seo, H., Lee, D. & Wang, X.J. (2011). A reservoir of time constants for memory traces in cortical neurons. Nature Neuroscience 14, 366–372.CrossRefGoogle ScholarPubMed
Bisley, J.W. & Pasternak, T. (2000). The multiple roles of visual cortical areas MT/MST in remembering the direction of visual motion. Cerebral Cortex 10, 1053–1065.CrossRefGoogle ScholarPubMed
Bisley, J.W., Zaksas, D. & Pasternak, T. (2001). Microstimulation of cortical area MT affects performance on a visual working memory task. Journal of Neurophysiology 85, 187–196.CrossRefGoogle ScholarPubMed
Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S. & Cohen, J.D. (2001). Conflict monitoring and cognitive control. Psychological Review 108, 624–652.CrossRefGoogle ScholarPubMed
Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. (1996). A relationship between behavioral choice and the visual responses of neurons in macaque MT. Visual Neuroscience 13, 87–100.CrossRefGoogle ScholarPubMed
Cai, X., Kim, S. & Lee, D. (2011). Heterogeneous coding of temporally discounted values in the dorsal and ventral striatum during intertemporal choice. Neuron 69, 170–182.CrossRefGoogle ScholarPubMed
Cai, X. & Padoa-Schioppa, C. (2012). Neuronal encoding of subjective value in dorsal and ventral anterior cingulate cortex. The Journal of Neuroscience 32, 3791–3808.CrossRefGoogle ScholarPubMed
Cohen, M.R. & Maunsell, J.H.R. (2009). Attention improves performance primarily by reducing interneuronal correlations. Nature Neuroscience 12, 1594–1600.CrossRefGoogle ScholarPubMed
Cohen, M.R. & Newsome, W.T. (2004). What electrical microstimulation has revealed about the neural basis of cognition. Current Opinion in Neurobiology 14, 169–177.CrossRefGoogle ScholarPubMed
Cohen, M.R. & Newsome, W.T. (2009). Estimates of the contribution of single neurons to perception depend on timescale and noise correlation. The Journal of Neuroscience 29, 6635–6648.CrossRefGoogle ScholarPubMed
Cook, E.P. & Maunsell, J.H. (2002). Dynamics of neuronal responses in macaque MT and VIP during motion detection. Nature Neuroscience 5, 985–994.CrossRefGoogle ScholarPubMed
Cromer, J.A., Roy, J.E., Buschman, T.J. & Miller, E.K. (2011). Comparison of primate prefrontal and premotor cortex neuronal activity during visual categorization. Journal of Cognitive Neuroscience 23, 3355–3365.CrossRefGoogle ScholarPubMed
DeAngelis, G.C. & Newsome, W.T. (2004). Perceptual “read-out” of conjoined direction and disparity maps in extrastriate area MT. PLoS Biology 2, e77.CrossRefGoogle ScholarPubMed
Dodd, J.V., Krug, K., Cumming, B.G. & Parker, A.J. (2001). Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area Mt. The Journal of Neuroscience 21, 4809–4821.CrossRefGoogle ScholarPubMed
Freedman, D.J., Riesenhuber, M., Poggio, T. & Miller, E.K. (2003). A comparison of primate prefrontal and inferior temporal cortices during visual categorization. The Journal of Neuroscience 23, 5235–5246.CrossRefGoogle ScholarPubMed
Glimcher, P. (2002). Decisions, decisions, decisions: Choosing a biological science of choice. Neuron 36, 323–332.CrossRefGoogle ScholarPubMed
Gottfried, J.A., O’Doherty, J. & Dolan, R.J. (2003). Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301, 1104–1107.CrossRefGoogle ScholarPubMed
Green, D.M. & Swets, J.A. (1966). Signal Detection Theory and Psychophysics. New York: Wiley.Google Scholar
Hayden, B.Y. & Gallant, J.L. (2013). Working memory and decision processes in visual area V4. Frontiers in Neuroscience 7, 1–10.CrossRefGoogle ScholarPubMed
Hayden, B.Y., Heilbronner, S.R., Nair, A.C. & Platt, M.L. (2008 a). Cognitive influences on risk-seeking by rhesus macaques. Judgment and Decision Making 3, 389–395.CrossRefGoogle ScholarPubMed
Hayden, B.Y., Heilbronner, S.R., Pearson, J.M. & Platt, M.L. (2011 a). Surprise signals in anterior cingulate cortex: Neuronal encoding of unsigned reward prediction errors driving adjustment in behavior. The Journal of Neuroscience 31, 4178–4187.CrossRefGoogle ScholarPubMed
Hayden, B.Y., Heilbronner, S.R. & Platt, M.L. (2010). Ambiguity aversion in rhesus macaques. Frontiers in Neuroscience 4, 1–7.CrossRefGoogle ScholarPubMed
Hayden, B.Y., Nair, A.C., McCoy, A.N. & Platt, M.L. (2008 b). Posterior cingulate cortex mediates outcome-contingent allocation of behavior. Neuron 60, 19–25.CrossRefGoogle ScholarPubMed
Hayden, B.Y., Pearson, J.M. & Platt, M.L. (2009 a). Fictive reward signals in the anterior cingulate cortex. Science 324, 948–950.CrossRefGoogle ScholarPubMed
Hayden, B.Y., Pearson, J.M. & Platt, M.L. (2011 b). Neuronal basis of sequential foraging decisions in a patchy environment. Nature Neuroscience 14, 933–939.CrossRefGoogle Scholar
Hayden, B.Y., Smith, D.V. & Platt, M.L. (2009 b). Electrophysiological correlates of default-mode processing in macaque posterior cingulate cortex. Proceedings of the National Academy of Sciences of the United States of America 106, 5948–5953.CrossRefGoogle ScholarPubMed
Hernández, A.N., Nácher, V., Luna, R., Zainos, A., Lemus, L., Alvarez, M., Vázquez, Y., Camarillo, L. & Romo, R. (2010). Decoding a perceptual decision process across cortex. Neuron 66, 300–314.CrossRefGoogle ScholarPubMed
Hunt, L.T., Kolling, N., Soltani, A., Woolrich, M.W., Rushworth, M.F. & Behrens, T.E. (2012). Mechanisms underlying cortical activity during value-guided choice. Nature Neuroscience 15, 470–476.CrossRefGoogle ScholarPubMed
Hussar, C. & Pasternak, T. (2010). Trial-to-trial variability of the prefrontal neurons reveals the nature of their engagement in a motion discrimination task. Proceedings of the National Academy of Sciences of the United States of America 107, 21842–21847.CrossRefGoogle Scholar
Hussar, C.R. & Pasternak, T. (2009). Flexibility of sensory representations in prefrontal cortex depends on cell type. Neuron 64, 730–743.CrossRefGoogle ScholarPubMed
Hussar, C.R. & Pasternak, T. (2012). Memory-guided sensory comparisons in the prefrontal cortex: Contribution of putative pyramidal cells and interneurons. The Journal of Neuroscience 32, 2747–2761.CrossRefGoogle ScholarPubMed
Hussar, C.R. & Pasternak, T. (2013). Common rules guide comparisons of speed and direction of motion in the dorsolateral prefrontal cortex. The Journal of Neuroscience 33, 972–986.CrossRefGoogle ScholarPubMed
Ito, S., Stuphorn, V., Brown, J.W. & Schall, J.D. (2003). Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302, 120–122.CrossRefGoogle ScholarPubMed
Jocham, G., Hunt, L.T., Near, J. & Behrens, T.E.J. (2012). A mechanism for value-guided choice based on the excitation-inhibition balance in prefrontal cortex. Nature Neuroscience 15, 960–961.CrossRefGoogle ScholarPubMed
Kennerley, S.W., Behrens, T.E.J. & Wallis, J.D. (2011). Double dissociation of value computations in orbitofrontal and anterior cingulate neurons. Nature Neuroscience 14, 1581–1589.CrossRefGoogle ScholarPubMed
Kennerley, S.W., Dahmubed, A.F., Lara, A.H. & Wallis, J.D. (2009). Neurons in the frontal lobe encode the value of multiple decision variables. Journal of Cognitive Neuroscience 21, 1162–1178.CrossRefGoogle ScholarPubMed
Kennerley, S.W. & Wallis, J.D. (2009). Evaluating choices by single neurons in the frontal lobe: Outcome value encoded across multiple decision variables. The European Journal of Neuroscience 29, 2061–2073.CrossRefGoogle ScholarPubMed
Kerns, J.G., Cohen, J.D., MacDonald, A.W. III, Cho, R.Y., Stenger, V.A. & Carter, C.S. (2004). Anterior cingulate conflict monitoring and adjustments in control. Science 303, 1023–1026.CrossRefGoogle ScholarPubMed
Krajbich, I., Armel, C. & Rangel, A. (2010). Visual fixations and the computation and comparison of value in simple choice. Nature Neuroscience 13, 1292–1298.CrossRefGoogle ScholarPubMed
Lara, A.H., Kennerley, S.W. & Wallis, J.D. (2009). Encoding of gustatory working memory by orbitofrontal neurons. The Journal of Neuroscience 29, 765–774.CrossRefGoogle ScholarPubMed
Leathers, M.L. & Olson, C.R. (2012). In monkeys making value-based decisions, LIP neurons encode cue salience and not action value. Science 338, 132–135.CrossRefGoogle Scholar
Liu, J. & Newsome, W.T. (2006). Local field potential in cortical area MT: Stimulus tuning and behavioral correlations. The Journal of Neuroscience 26, 7779–7790.CrossRefGoogle ScholarPubMed
Lui, L.L. & Pasternak, T. (2011). Representation of comparison signals in cortical area MT during a delayed direction discrimination task. Journal of Neurophysiology 106, 1260–1273.CrossRefGoogle ScholarPubMed
Matsumoto, M., Matsumoto, K., Abe, H. & Tanaka, K. (2007). Medial prefrontal cell activity signaling prediction errors of action values. Nature Neuroscience 10, 647–656.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. (2004). Neuronal representations of cognitive state: reward or attention? Trends in Cognitive Sciences 8, 261–265.CrossRefGoogle ScholarPubMed
Miller, E.K. & Cohen, J.D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience 24, 167–202.CrossRefGoogle ScholarPubMed
Miller, E.K., Erickson, C.A. & Desimone, R. (1996). Neural mechanisms of visual working memory in prefrontal cortex of the macaque. The Journal of Neuroscience 16, 5154–5167.CrossRefGoogle ScholarPubMed
Miller, E.K., Li, L. & Desimone, R. (1993). Activity of neurons in anterior inferior temporal cortex during a short-term memory task. The Journal of Neuroscience 13, 1460–1478.CrossRefGoogle ScholarPubMed
Montague, P.R. & Berns, G.S. (2002). Neural economics and the biological substrates of valuation. Neuron 36, 265–284.CrossRefGoogle ScholarPubMed
Newsome, W.T., Britten, K.H. & Movshon, J.A. (1989). Neuronal correlates of a perceptual decision. Nature 341, 52–54.CrossRefGoogle ScholarPubMed
Nichols, M.J. & Newsome, W.T. (2002). Middle temporal visual area microstimulation influences veridical judgments of motion direction. The Journal of Neuroscience 22, 9530–9540.CrossRefGoogle ScholarPubMed
Niki, H. & Watanabe, M. (1979). Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Research 171, 213–224.CrossRefGoogle ScholarPubMed
Ninomiya, T., Sawamura, H., Inoue, K.I. & Takada, M. (2012). Segregated pathways carrying frontally derived top-down signals to visual areas MT and V4 in macaques. The Journal of Neuroscience 32, 6851–6858.CrossRefGoogle ScholarPubMed
Padoa-Schioppa, C. (2011). Neurobiology of economic choice: A good-based model. Annual Review of Neuroscience 34, 333–359.CrossRefGoogle Scholar
Padoa-Schioppa, C. & Assad, J.A. (2006). Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223–226.CrossRefGoogle ScholarPubMed
Palmer, C., Cheng, S.Y. & Seidemann, E. (2007). Linking neuronal and behavioral performance in a reaction-time visual detection task. The Journal of Neuroscience 27, 8122–8137.CrossRefGoogle Scholar
Parker, A.J., Krug, K. & Cumming, B.G. (2002). Neuronal activity and its links with the perception of multi-stable figures. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 357, 1053–1062.CrossRefGoogle ScholarPubMed
Pasternak, T. & Greenlee, M. (2005). Working memory in primate sensory systems. Nature Reviews. Neuroscience 6, 97–107.CrossRefGoogle ScholarPubMed
Paton, J.J., Belova, M.A., Morrison, S.E. & Salzman, C.D. (2006). The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature 439, 865–870.CrossRefGoogle ScholarPubMed
Petrides, M. & Pandya, D.N. (2006). Efferent association pathways originating in the caudal prefrontal cortex in the macaque monkey. The Journal of Comparative Neurology 498, 227–251.CrossRefGoogle ScholarPubMed
Platt, M.L. & Glimcher, P.W. (1999). Neural correlates of decision variables in parietal cortex. Nature 400, 233–238.CrossRefGoogle ScholarPubMed
Rangel, A., Camerer, C. & Montague, P.R. (2008). A framework for studying the neurobiology of value-based decision making. Nature Reviews. Neuroscience 9, 545–556.CrossRefGoogle ScholarPubMed
Roesch, M.R. & Olson, C.R. (2004). Neuronal activity related to reward value and motivation in primate frontal cortex. Science 304, 307–310.CrossRefGoogle ScholarPubMed
Romo, R. & Salinas, E. (2003). Flutter discrimination: Neural codes, perception, memory and decision making. Nature Reviews. Neuroscience. 4, 203–218.CrossRefGoogle ScholarPubMed
Rushworth, M.F.S., Noonan, M.A.P., Boorman, E.D., Walton, M.E. & Behrens, T.E. (2011). Frontal cortex and reward-guided learning and decision-making. Neuron 70, 1054–1069.CrossRefGoogle ScholarPubMed
Sallet, J., Quilodran, R., Rothe, M., Vezoli, J., Joseph, J.P. & Procyk, E. (2007). Expectations, gains, and losses in the anterior cingulate cortex. Cognitive, Affective and Behavioral Neuroscience 7, 327–336.CrossRefGoogle ScholarPubMed
Salzman, C.D., Britten, K.H. & Newsome, W.T. (1990). Cortical microstimulation influences perceptual judgements of motion direction. Nature 346, 174–177[published erratum appears in Nature 1990 Aug 9;346(6284):589] [see comments].CrossRefGoogle ScholarPubMed
Schultz, W. (2006). Behavioral theories and the neurophysiology of reward. Annual Review of Psychology 57, 87–115.CrossRefGoogle ScholarPubMed
Seo, H. & Lee, D. (2007). Temporal filtering of reward signals in the dorsal anterior cingulate cortex during a mixed-strategy game. The Journal of Neuroscience 27, 8366–8377.CrossRefGoogle ScholarPubMed
Shidara, M. & Richmond, B.J. (2002). Anterior cingulate: Single neuronal signals related to degree of reward expectancy. Science 296, 1709–1711.CrossRefGoogle ScholarPubMed
Shiozaki, H.M., Tanabe, S., Doi, T. & Fujita, I. (2012). Neural activity in cortical area V4 underlies fine disparity discrimination. The Journal of Neuroscience 32, 3830–3841.CrossRefGoogle ScholarPubMed
Uchida, N., Kepecs, A. & Mainen, Z.F. (2006). Seeing at a glance, smelling in a whiff: Rapid forms of perceptual decision making. Nature Reviews. Neuroscience 7, 485–491.CrossRefGoogle Scholar
Uka, T. & DeAngelis, G.C. (2004). Contribution of area MT to stereoscopic depth perception: Choice-related response modulations reflect task strategy. Neuron 42, 297–310.CrossRefGoogle ScholarPubMed
Wallis, J.D. (2007). Orbitofrontal cortex and its contribution to decision-making. Annual Review of Neuroscience 30, 31–56.CrossRefGoogle ScholarPubMed
Walton, M.E., Bannerman, D.M., Alterescu, K. & Rushworth, M.F. (2003). Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. The Journal of Neuroscience 23, 6475–6479.CrossRefGoogle ScholarPubMed
Wang, X.J. (2012). Neural dynamics and circuit mechanisms of decision-making. Current Opinion in Neurobiology 22, 1039–1046.CrossRefGoogle ScholarPubMed
Williams, Z.M., Bush, G., Rauch, S.L., Cosgrove, G.R. & Eskandar, E.N. (2004). Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nature Neuroscience 7, 1370–1375.CrossRefGoogle ScholarPubMed
Zaksas, D. & Pasternak, T. (2006). Directional signals in the prefrontal cortex and in area MT during a working memory for visual motion task. The Journal of Neuroscience 26, 11726–11742.CrossRefGoogle ScholarPubMed