Decision Making: Remembering to choose the future

A brain region known as the hippocampus is required when people assess different options before making a value-based choice.
  1. Lesley K Fellows  Is a corresponding author
  1. McGill University, Canada

From the philosophers of ancient Greece to the self-help books of today, humans have long been interested in choice. Philosophers and ethicists have debated what goals we ought to choose for millennia, and for a century or more economists and psychologists have studied what goals we will choose. However, neuroscience has only recently begun to systematically address how we choose.

Whether we are pondering life-defining decisions about love, career or commitment to a cause, or simply picking which snacks to buy in the grocery store, it is still unclear what regions of the brain are involved in making choices, and what information those regions encode. In everyday language, we often talk about ‘value’ (or in economic terms, ‘utility’) as the driver of such decisions: we consider our options, and select the one with the highest value. Hundreds of functional MRI (or fMRI) studies in healthy humans have identified a consistent set of brain regions which seem to process signals associated with subjective values; this suggests that value is indeed a concept that has biological roots (Bartra et al., 2013). However, the nature of the information that contributes to the neural signals related to value remains a matter of debate (O'Doherty, 2014). In other words, it is not clear what we think about when we think about value.

In fact, scientists know far less about choices based on value than they do about perceptual decisions (such as assessing if a noisy array of moving dots is trending more to the left or to the right; Shadlen and Kiani, 2013). During perceptual choices, external information is repeatedly sampled and the neural representation of this evidence accumulates until a threshold is crossed and a decision is triggered. These tasks are associated with well-known behavioral phenomena – for instance, choices with less perceptual evidence take longer to resolve – which are captured by drift diffusion models (Ratcliff and McKoon, 2008).

It has been proposed that value-based decisions might occur in a similar way (Rangel et al., 2008). However, while it is obvious what knowledge is accumulating as a person gazes at a screen filled with moving dots, it is less clear what information might be sampled to support a decision based on value. Now, in eLife, Akram Bakkour of Columbia University and colleagues report that, at least in part, we may be thinking about past experiences (Bakkour et al., 2019).

Their work makes a strong case that value-based deliberation engages the hippocampus, a small structure within the brain that is involved in long-term memory. Although past experiences are a likely source of relevant information in value-based decisions, to date researchers have focused mostly on other regions of the brain such as the ventral prefrontal cortex and the striatum.

Bakkour et al. – who are based at Columbia and the Memory Disorders Research Center – first used fMRI to establish that activity in the hippocampus is greater for longer deliberations during value-based choice. They then harnessed the power of a lesion experiment to infer that the structure is necessary for such choices (Vaidya et al., 2019). Patients with hippocampal damage were slower to make decisions, and somewhat more variable in what they chose. These hippocampal effects were specific to value-based decisions. Deliberation time in a classic perceptual decision task did not relate to hippocampal signal, nor was it influenced by hippocampal damage. While perceptual decisions involve sampling external evidence, Bakkour et al. propose that deliberation during value-based choice requires sampling internal evidence. This includes – although is presumably not limited to – using the hippocampus to conjure up past experiences with similar options. Ultimately, these results will help to broaden the anatomical scope of decision neuroscience.

Studies have already shown that ‘attention’, while intuitive and attractive as a holistic concept, is in fact composed of dozens of distinct processes with definable characteristics that rely on different neural circuits. It is likely that ‘value’ will also require further decomposition. Armed with this knowledge, it may become possible to better understand how the brain carries out the important value-based decisions that define us as individuals and shape the directions of our societies.

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Author details

  1. Lesley K Fellows

    Lesley K Fellows is in the Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, Canada

    For correspondence
    lesley.fellows@mcgill.ca
    Competing interests
    No competing interests declared
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9144-092X

Publication history

  1. Version of Record published: August 14, 2019 (version 1)

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© 2019, Fellows

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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  1. Lesley K Fellows
(2019)
Decision Making: Remembering to choose the future
eLife 8:e49828.
https://doi.org/10.7554/eLife.49828
  1. Further reading

Further reading

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    Functional interactions between the prefrontal cortex and hippocampus, as revealed by strong oscillatory synchronization in the theta (6–11 Hz) frequency range, correlate with memory-guided decision-making. However, the degree to which this form of long-range synchronization influences memory-guided choice remains unclear. We developed a brain-machine interface that initiated task trials based on the magnitude of prefrontal-hippocampal theta synchronization, then measured choice outcomes. Trials initiated based on strong prefrontal-hippocampal theta synchrony were more likely to be correct compared to control trials on both working memory-dependent and -independent tasks. Prefrontal-thalamic neural interactions increased with prefrontal-hippocampal synchrony and optogenetic activation of the ventral midline thalamus primarily entrained prefrontal theta rhythms, but dynamically modulated synchrony. Together, our results show that prefrontal-hippocampal theta synchronization leads to a higher probability of a correct choice and strengthens prefrontal-thalamic dialogue. Our findings reveal new insights into the neural circuit dynamics underlying memory-guided choices and highlight a promising technique to potentiate cognitive processes or behavior via brain-machine interfacing.

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    Hippocampal place cells in freely moving rodents display both theta phase precession and procession, which is thought to play important roles in cognition, but the neural mechanism for producing theta phase shift remains largely unknown. Here, we show that firing rate adaptation within a continuous attractor neural network causes the neural activity bump to oscillate around the external input, resembling theta sweeps of decoded position during locomotion. These forward and backward sweeps naturally account for theta phase precession and procession of individual neurons, respectively. By tuning the adaptation strength, our model explains the difference between ‘bimodal cells’ showing interleaved phase precession and procession, and ‘unimodal cells’ in which phase precession predominates. Our model also explains the constant cycling of theta sweeps along different arms in a T-maze environment, the speed modulation of place cells’ firing frequency, and the continued phase shift after transient silencing of the hippocampus. We hope that this study will aid an understanding of the neural mechanism supporting theta phase coding in the brain.