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

Nature. 2016 Jul 14;535(7611):285-8. doi: 10.1038/nature18617. Epub 2016 Jul 4.

Abstract

During decision making, neurons in multiple brain regions exhibit responses that are correlated with decisions. However, it remains uncertain whether or not various forms of decision-related activity are causally related to decision making. 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 making, 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 encoding. 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.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Choice Behavior / physiology
  • Decision Making / physiology*
  • Discrimination, Psychological
  • Eye Movements / physiology
  • Female
  • Macaca mulatta / anatomy & histology*
  • Macaca mulatta / physiology*
  • Macaca mulatta / psychology
  • Male
  • Models, Neurological*
  • Motion Perception / physiology
  • Neurons / physiology
  • Parietal Lobe / cytology
  • Parietal Lobe / physiology
  • Photic Stimulation
  • Psychophysiology
  • Temporal Lobe / cytology
  • Temporal Lobe / physiology