Neurons in the Primate Medial Basal Forebrain Signal Combined Information about Reward Uncertainty, Value, and Punishment Anticipation

Abstract

It has been suggested that the basal forebrain (BF) exerts strong influences on the formation of memory and behavior. However, what information is used for the memory-behavior formation is unclear. We found that a population of neurons in the medial BF (medial septum and diagonal band of Broca) of macaque monkeys encodes a unique combination of information: reward uncertainty, expected reward value, anticipation of punishment, and unexpected reward and punishment. The results were obtained while the monkeys were expecting (often with uncertainty) a rewarding or punishing outcome during a Pavlovian procedure, or unexpectedly received an outcome outside the procedure. In vivo anterograde tracing using manganese-enhanced MRI suggested that the major recipient of these signals is the intermediate hippocampal formation. Based on these findings, we hypothesize that the medial BF identifies various contexts and outcomes that are critical for memory processing in the hippocampal formation.

Microscopic and mesoscopic effects of reward uncertainty in monkey fronto-parietal areas

“…Together, these findings support the conclusion that the brain explicitly signals uncertainty as a bona-fide quantity rather than merely a secondary aspect of reward distributions. This conclusion is consistent with previous findings in subcortical structures and the orbitofrontal cortex [27][28][29] , and our results show that it extends to the fronto-parietal network involved in cognitive regulation.…”

“…The traces from each session were then pooled and subjected to a two-step cleaning procedure to remove outliers in, respectively, the frequency and time domains. For the first step that removed outliers in the frequency domain, we calculated the power spectrum of each LFP trace in the range of 0 -90 Hz (using a multi-taper method with 4 tapers) and characterized each trial with a 5-dimensional vector containing the sum of the logarithm of the power spectrum in 5 frequency bands (0.5-4 Hz, 4-8 Hz, [8][9][10][11][12][12][13][14][15][16][17][18][19][20][21][22][23][24][25][26][27][28][29][30] Hz and 30-90 Hz). We then reduced the dimensionality of each session's data set to 2 principal components using principal component analysis, and clustered this 2dimensional data set using Gaussian Mixture Models (GMM; fitgmdist function in the MATLAB statistics and machine learning toolbox).…”

“…Specifically, uncertainty acts as a trigger for initiating cognitive actionssuch as enhanced learning rates 23 and attentional orienting 24,25 aimed to reduce the uncertainty. Reward uncertainty is encoded independently of expected value (EV) in dopamine cells 26 , the orbitofrontal cortex 27 , the anterodorsal septum 28 and the basal forebrain 29 . But it remains unknown whether, and how, it is encoded in frontal and parietal areas involved in attention regulation.…”

The menagerie of the basal forebrain: how many (neural) species are there, what do they look like, how do they behave and who talks to whom?

“…The basal forebrain (BF) is a large heterogeneous structure located close to the ventral surface of the rostral telencephalon (Figure 1) which is involved in sleep-wake control, attention and reward processing [1–3]. Until relatively recently, most of these functions were ascribed to the BF cholinergic neurons which degenerate in Alzheimer’s disease and other dementias [4].…”

Anterior cingulate is a source of valence-specific information about value and uncertainty

“…6a, see refs 55–57, 63 ) indicating they understood the meanings of the CSs. After training, 58 ACC reward uncertainty enhanced neurons were identified and studied in the single CS reward probability/reward amount behavioral procedure.

Fig.

…”