Frontal Cortex Neuron Types Encode Decision Variables
Nature 576, pages446–451(2019)
Frontal cortex neuron types categorically encode single decision variables
Junya Hirokawa, et.al.
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, US
Graduate School of Brain Science, Doshisha University, Kyotanabe, Kyoto, Japan
Watson School of Biological Sciences, Cold Spring Harbor, NY, USA
[paraphrase]
Individual neurons in many cortical regions have been found to encode specific,
identifiable features of the environment or body that pertain to the function of the
region. However, in frontal cortex, which is involved in cognition, neural responses
display baffling complexity, carrying seemingly disordered mixtures of sensory, motor
and other task-related variables. This complexity has led to the suggestion that
representations in individual frontal neurons are randomly mixed and can only be
understood at the neural population level. Here we show that neural activity in rat
orbitofrontal cortex (OFC) is instead highly structured: single neuron activity co-
varies with individual variables in computational models that explain choice behaviour.
To characterize neural responses across a large behavioural space, we trained rats on a
behavioural task that combines perceptual and value-guided decisions. An unbiased,
model-free clustering analysis identified distinct groups of OFC neurons, each with a
particular response profile in task-variable space. Applying a simple model of choice
behaviour to these categorical response profiles revealed that each profile quantitatively
corresponds to a specific decision variable, such as decision confidence. Additionally, we
demonstrate that a connectivity-defined cell type, orbitofrontal neurons projecting to
the striatum, carries a selective and temporally sustained representation of a single
decision variable: integrated value. We propose that neurons in frontal cortex, as in
other cortical regions, form a sparse and overcomplete representation of features
relevant to the region’s function, and that they distribute this information selectively
to downstream regions to support behaviour.
The brain represents the external world in patterns of neural activity that guide
adaptive behaviour. In many regions, individual cortical neurons respond to features,
such as visual edges, objects or spatial locations, that reflect regional function. When
examining frontal areas engaged in decision making, however, one is struck most of all
by the complexity and diversity of their neuronal responses. The difficulty in
identifying structure in frontal cortical representations probably reflects the fact that
cognitive variables are more challenging to define than simpler features such as visual
edges. It is further challenging to design behavioural tasks that engage the specific
cognitive functions of frontal cortical neurons to sufficiently probe the relevant feature
space. As a result, it is unclear whether frontal cortex representations are
comprehensible in single neurons or instead require neural population analysis
We used a behavioural task that combines perceptual and value-guided decision making
to demonstrate that OFC representations are highly structured: encoding a small set
of categorical representations that correspond to coherent decision variables in
specific task epochs. The functionally homogeneous encoding of decision variables by
OFC–STR neurons further suggests that OFC response diversity is partly due to cell-type-
specific organization. Sustained firing of OFC–STR neurons across trials encoded value,
potentially a neural correlate of a temporal credit assignment mechanism. Alongside
neuron-type-specific recordings in cortical and subcortical areas during behaviour,
this result exposes an intimate connection between the functional and anatomical
organization of cortex supporting computation.