Cortical and basal ganglia contributions to habit learning and automaticity

Abstract

In the 20th century it was thought that novel behaviors are mediated primarily in cortex and that the development of automaticity is a process of transferring control to subcortical structures. However, evidence supports the view that subcortical structures, such as the striatum, make significant contributions to initial learning. More recently, there has been increasing evidence that neurons in the associative striatum are selectively activated during early learning, whereas those in the sensorimotor striatum are more active after automaticity has developed. At the same time, other recent reports indicate that automatic behaviors are striatum- and dopamine-independent, and might be mediated entirely within cortex. Resolving this apparent conflict should be a major goal of future research.

Figure 1

Responses of one neuron in the associative striatum and one neuron in the sensorimotor striatum of a monkey during the performance of a new and an old motor sequence. The monkey's task was to depress a sequence of ten buttons in a predetermined order. In each case, the recordings shown here were to a movement from the key with the white dot to the black key. The vertical lines indicate the time at which the key with the white dot was depressed. In the associative striatum, more than twice as many neurons were found that responded to new sequences more strongly than to old sequences (i.e., 40% versus 18%), whereas in the sensorimotor striatum almost twice as many neurons were found that responded more strongly to old sequences than to new sequences (i.e., 30% versus 17%) (adapted with permission from [14]).

Figure 2

Spike histograms from single cells in the sensorimotor striatum of a rat in a task in which it is trained to lever press to a tone (reprinted with permission from [22]). The vertical line denotes the time of the lever press. Note that the time axis is defined relative to the lever press, rather than the tone onset.

Figure 3

Cortico-striatal inputs (S_A, S_B) coding for sensory events synapse upon striatal output neurons that eventually lead to behavioral responses (R_A, R_B). A behavioral response (R_A) leading to delivery of a reward or reward-predicting stimulus causes a phasic increase in midbrain dopamine activity and a consequent increase in striatal dopamine release. Dopamine-mediated LTP strengthens the currently-active synapses (S_B to R_A; bottom diagram, bold box in striatum) and increases the likelihood that the reward-procuring behavioral response (R_A) will occur in response to the same sensory stimulus (S_B) in the future. (Reprinted with permission from [37]).

Figure I

(Box 2) Schematic diagram of the basal ganglia and its afferents and efferents. Black lines terminating in arrowheads are excitatory, those terminating in filled circles are inhibitory, and gray lines terminating in squares are dopaminergic. All structures are part of the basal ganglia except cortex and thalamus. PFC = prefrontal cortex; SMA = supplementary motor area; GP_e = external segment of the globus pallidus; GP_i = internal segment of the globus pallidus; MD = medial dorsal nucleus; VA = ventral anterior nucleus; VL = ventral lateral nucleus; STN = subthalamic nucleus; SNpc = substantia nigra pars compacta; SNpr = substantia nigra pars reticulata.