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Dissociated functional significance of decision-related activity in the primate dorsal stream

Nature volume 535, pages 285–288 (2016)Cite this article

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Abstract

During decision making, neurons in multiple brain regions exhibit responses that are correlated with decisions1,2,3,4,5,6. However, it remains uncertain whether or not various forms of decision-related activity are causally related to decision making7,8,9. Here we address this question by recording and reversibly inactivating the lateral intraparietal (LIP) and middle temporal (MT) areas of rhesus macaques performing a motion direction discrimination task. Neurons in area LIP exhibited firing rate patterns that directly resembled the evidence accumulation process posited to govern decision making2,10, with strong correlations between their response fluctuations and the animal’s choices. Neurons in area MT, in contrast, exhibited weak correlations between their response fluctuations and choices, and had firing rate patterns consistent with their sensory role in motion encoding1. The behavioural impact of pharmacological inactivation of each area was inversely related to their degree of decision-related activity: while inactivation of neurons in MT profoundly impaired psychophysical performance, inactivation in LIP had no measurable impact on decision-making performance, despite having silenced the very clusters that exhibited strong decision-related activity. Although LIP inactivation did not impair psychophysical behaviour, it did influence spatial selection and oculomotor metrics in a free-choice control task. The absence of an effect on perceptual decision making was stable over trials and sessions and was robust to changes in stimulus type and task geometry, arguing against several forms of compensation. Thus, decision-related signals in LIP do not appear to be critical for computing perceptual decisions, and may instead reflect secondary processes. Our findings highlight a dissociation between decision correlation and causation, showing that strong neuron-decision correlations do not necessarily offer direct access to the neural computations underlying decisions.

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Figure 1: Task and neural responses during direction discrimination.
Figure 2: Psychophysical performance before and after neural inactivations in areas MT and LIP.
Figure 3: Performance in control tasks following LIP inactivation.

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Acknowledgements

We thank R. Krauzlis, C. Brody, E. Seidemann, L. Cormack, and R. Aldrich for comments on the manuscript. We thank the Brody laboratory (particularly C. Brody and J. Erlich) for inspiring the experiments, the Mauk laboratory (particularly M. Mauk, F. Riusech, and H. Halverson) for assistance with muscimol preparation, and K. Mitchell for animal support. This research was supported by the Howard Hughes Medical Institute International Student Research Fellowship to L.N.K., the McKnight Foundation grant to J.W.P., the National Eye Institute (R01-EY017366) grant to both J.W.P, and A.C.H., and the National Institutes of Health under Ruth L. Kirschstein National Research Service Awards T32DA018926 from the National Institute on Drug Abuse and T32EY021462 from the National Eye Institute.

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Author notes

  1. Leor N. Katz and Jacob L. Yates: These authors contributed equally to this work.

Authors and Affiliations

  1. Departments of Neuroscience & Psychology, Center for Perceptual Systems, The University of Texas at Austin, Austin, 78712, Texas, USA

    Leor N. Katz, Jacob L. Yates & Alexander C. Huk

  2. Princeton Neuroscience Institute & Department of Psychology, Princeton University, Princeton, 08540, New Jersey, USA

    Jonathan W. Pillow

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Contributions

L.N.K., J.L.Y. and A.C.H. designed the experiments. L.N.K. and J.L.Y. collected behavioural and electrophysiological data. L.N.K. and J.L.Y. performed pharmacological inactivations. L.N.K. analysed behavioural data. J.L.Y. analysed electrophysiological data. J.W.P. and A.C.H. guided data analysis. All authors discussed the results and wrote the manuscript.

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Correspondence to Leor N. Katz.

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Extended data figures and tables

Extended Data Figure 1 Location of LIP recording and muscimol infusion sites.

a, b, The recording (blue circles) and infusion sites (red) for monkey N (a) and monkey P (b) along the medial-lateral (M/L) and posterior-anterior (P/A) axes within the chamber (demarcated by the ovals). Electrode and cannula tracks are represented by the grey lines (with a small jitter on the x–y plane for better visualization). The mean infusion depths were 7.12 ± 1.15 mm (monkey N) and 7.03 ± 1.39 mm (monkey P) (the microdrive was zeroed below dura mater and just above the cortical surface). Given the estimated spread of muscimol described in the main text, the inactivations targeted a substantial territory of the ventral portion of LIP49. Even though a functional distinction with depth has been proposed34, we emphasize that the critical component of our protocol was targeting the precise locations at which we measured canonical decision-related activity in LIP.

Extended Data Figure 2 Direction discrimination sensitivity is restored when motion is placed outside of the inactivated MT field.

a. Illustration of MT inactivation along with the estimated inactivated field (grey cloud), for two experimental geometries: motion stimulus placed inside the inactivated MT field (top) and motion placed outside the inactivated MT field (bottom). b. Average psychophysical data for baseline and muscimol treatment pairs (grey and green, respectively, same data as Fig. 2c, n = 6; 3 in monkey N; 3 in monkey P) and psychophysical data collected during muscimol treatment, with the motion stimulus outside of the inactivated MT field (orange, n = 3). Direction discrimination sensitivity is restored to baseline levels in these sessions. Error bars on points show ± 1 s.e.m. over all trials.

Extended Data Figure 3 No relationship between effect magnitude in control task, effect magnitude in direction discrimination task, and muscimol mass.

a, b, The relationship between the effect of LIP inactivation in the free-choice task (that is, shift in proportion of contralateral choices from baseline to muscimol treatment) and the effect of LIP inactivation in the direction discrimination task on sensitivity (percentage change in psychometric function slope, a) and bias (shift in normalized motion strength, b). R2 and associated P values of a Pearson correlation are indicated on individual plots (n = 21; 12 in monkey N; 9 in monkey P). Orange data points indicate sessions in which muscimol was infused from two cannulae simultaneously into LIP. c–e, Dose–response functions between muscimol mass and the effect in the direction discrimination task on slope (c, same units as a), bias (d, same units as b), and the effect in the free-choice task (e, same units as a, b). For e, we used free-choice sessions that took place on the same days as the direction discrimination task (n = 21) along with an additional 13 sessions that took place during other inactivation experiments under similar conditions (n = 34 in total; 14 in monkey N; 20 in monkey P; as in Fig. 3d). R2, associated P values and regression lines are indicated on the plots (linear regression).

Extended Data Figure 4 Time course of accuracy and bias within sessions.

Accuracy and bias in the direction discrimination task were computed over time by taking a running mean of correct and contralateral choices, respectively (sliding window of 40 trials). a, Inactivation in area MT (n = 6, green curve; 3 in monkey N; 3 in monkey P) had a clear and consistent impact on behavioural accuracy compared to baseline (n = 6, grey), but did not have systematic effects on bias (bottom), consistent with our results from the fitted psychometric functions (main text). Panels show data from trial 40 (sliding window size) to the median trial length of each group of experiments (variable session lengths contribute to increased variability at later trials). Error bars show ± 1 s.e.m. between sessions. b, Inactivations in area LIP (n = 21, blue curve; 12 in monkey N; 9 in monkey P) yielded no systematic trends in either accuracy (top) or bias (bottom) compared to baseline (n = 21, grey), indicating that within-session compensation is unlikely. Panel format same as in a. We also investigated whether compensation may have taken place before we began collecting the ‘inactivation’ data set, or during the first 10–30 instruction (warm-up) trials. On 13 of the 21 LIP inactivation sessions, we collected a third data set (in addition to the standard paired baseline and inactivation data sets), in which psychophysical performance was monitored during the time muscimol was being infused (during infusion, orange curve). No systematic changes in accuracy or bias were observed in this exploratory data set either, further arguing against compensation on the time scales of our manipulations and measurements.

Extended Data Figure 5 Psychophysical performance in the direction discrimination task across sessions.

Panels show data from monkey P (left) and monkey N (right), for all baseline and treatment pairs: muscimol (blue, n = 21), saline (unfilled grey, n = 6) and sham (filled grey, n = 3). Each pair consists of two sessions that took place in close succession (typically on consecutive days), at a similar time of day, after a similar number of preceding tasks and trials, and is represented by two markers connected by a line. Additional control pairs with no saline/sham manipulation (n = 16) are not presented, for visual clarity. a, Psychometric function slope over sessions. No significant change in slope was present over time, evaluated by linear regression, for either monkey P (P = 0.22) or N (P = 0.63). When considering the difference in slope between baseline and treatment pairs, monkey P exhibited a small decrease (regression line slope = −0.07, P = 0.023). However, a similar effect was seen in the interleaved controls (saline and sham, grey markers), indicating that this pattern likely reflects nonspecific trends in performance across back-to-back pairs of experiments. Monkey N had no significant change (P = 0.92). b, Psychometric function midpoint over sessions. No significant change was observed in the session-to-session midpoint values, evaluated by linear regression, for either monkey P (P = 0.44) or monkey N (P = 0.24). When considering the difference in midpoint value for each data set pair over time (that is, muscimol treatment – baseline), no significant change was detected either (P = 0.98 and P = 0.4 for monkey P and N, respectively). The x axis dates are in the year, month, date, yyyymmdd format.

Extended Data Figure 6 Psychophysical performance for all individual baseline and treatment session pairs.

a–c, All pairs of baseline and treatment sessions for all treatment types: muscimol, saline, and sham, (control pairs with no saline/sham manipulation are similar but not presented, for visual clarity) for all variants of the direction discrimination task: standard geometry (a), both targets in inactivated field (b), and Newsome dots (c), for both LIP and MT inactivation. In all panels, the abscissa represents motion strength towards the direction contralateral to the LIP under study, the ordinate represents the proportion of contralateral choices. The grey curve is baseline, and the coloured curve is treatment. The first panel in each section presents mean psychophysical performance for each monkey over sessions. Subsequent panels present individual session pairs. Error bars are s.e.m. over all trials.

Extended Data Table 1 Parametric and nonparametric analysis of psychophysical data, for two- and four-parameter psychometric functions
Full size table
Extended Data Table 2 Infusion details for all treatment sessions
Full size table

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Katz, L., Yates, J., Pillow, J. et al. Dissociated functional significance of decision-related activity in the primate dorsal stream. Nature 535, 285–288 (2016). https://doi.org/10.1038/nature18617

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