The role of striatum in initiation and execution of learned action sequences in rats

Abstract

To understand the role of striatum in motor sequence learning, we trained rats to perform a series of tasks measuring speed and accuracy of responding to luminance cues presented as discriminative stimuli for single nose pokes or for sequences of nose pokes in a serial reaction time task. Habit (stimulus-response) learning was measured by comparing performances when stimuli were repeated (predictable) with when they were selected randomly (unpredictable). Sequences had defined start and end points and were limited to five nose pokes to minimize chunking. When sequences were repeated, response time (RT) increased for nose pokes initiating the sequence and decreased for nose pokes completing it. These effects developed incrementally across sessions, consistent with the time course of habit learning. Medial (mCPu), lateral, and complete (CPu) caudate-putamen lesions affected speed and accuracy of single nose poke responses, confirming the role of these areas in guiding responses with external sensory stimuli. None of these lesions affected the short-term increase in accuracy observed when single nose poke responses were repeated. Both mCPu and CPu lesions increased RTs for initiating sequential responses, effects that were exacerbated across sessions in which specific sequences were repeated. None of the lesions affected the gradual decrease in RT for nose pokes completing repeated sequences. Correlational analyses confirmed the relationship between the extent of dorsal striatal damage and the ability to respond to brief luminance cues and to initiate learned sequences. These results provide evidence implicating dorsal striatum in higher-level organizational aspects of learning reflected in planning that precedes the execution of learned action sequences.

Figure 1.

Scaled drawing of the apparatus used for behavioral training. For all tasks, trials began with a press of the retractable lever. Luminance cues (from lights centered at the back of each port) were then triggered when rats next crossed the photocell before entering the main chamber. Water was delivered in wells in the floors of response ports to reinforce correct responding.

Figure 2.

Photomicrographs of representative striatal lesions ∼1 mm anterior to bregma in the coronal plane. A, A complete CPu lesion; B, a medial mCPu lesion; C, a ventral VSt lesion; D, a lateral lCPu lesion; E, control caudate–putamen; F, control ventral striatum. Scale bar: (in A) A–F, 1 mm. LV, Lateral ventricle; ec, external capsule; cc, corpus callosum; aca, anterior commissure, anterior part; Pir, piriform cortex; Tu, olfactory tubercle; C, core area of nucleus accumbens; Sh, shell area of nucleus accumbens. See Materials and Methods for descriptions of the lesions.

Figure 3.

Drawings of the largest (unfilled) and smallest (filled) amounts of damage produced by each of the four lesions. The drawings are based on quantitative measurements at 0.5 mm from bregma (see Materials and Methods for details). Drawings are on templates derived from Paxinos and Watson (1998) with permission from the publisher.

Figure 4.

Effects of striatal lesions on response accuracy, RT, and types of errors made in the basic RT task. A, Accuracy is plotted as percentage correct of responses (excluding omissions) at each of the stimulus durations tested. B, Runway RT (from the lever press until the runway photo beam was broken) and choice RT (from the photo beam break until a choice response was made). RT was measured as the median for each animal for correct responses only. C, The overall percentages of responses that were correct, errors of omission (not responding within the limited hold), and errors of commission (incorrect responses within the limited hold). Error bars represent SEM.

Figure 5.

Short-term learning plotted as percentage correct for blocks of seven trials in which the location of the S+ port was held constant. Stimulus duration was 0.05 s for trials 1, 3, 5, and 7 and 3.0 s for trials 2, 4, and 6 of each block. Rats with CPu lesions did not complete a sufficient number of trials for inclusion in analyses. There were few errors for 3.0 s stimuli. Percentage correct for the 0.05 s stimuli increased incrementally as they were repeated. Rats in the mCPu group were less accurate on average but exhibited increased accuracy with repetition comparable with other groups. The performances of the control, VSt, and lCPu groups were highly similar and thus overlap extensively in this figure. Error bars represent SEM.

Figure 6.

RT to make initial nose pokes in single nose poke and five nose poke serial reaction time responses. Results are presented for sessions in which discriminative stimuli changed randomly on each trial (random) and in which they were repeated unchanged on every trial (repeat). All groups were faster initiating single nose pokes than five nose poke sequences and sequences that were unpracticed (random) than those that were well practiced (repeat). These effects were exacerbated for rats with mCPu and CPu lesions. Error bars represent SEM.

Figure 7.

Incremental changes in RT for repeated serial reaction time sequences. A, B, The effects of repetition during the initial session in which sequence A was repeated. This was measured for individual animals by dividing sessions R1 and A1 into five blocks of 12 responses and subtracting median RTs for R1 from A1. Positive values indicate increased RT for the repeated sequence. Results are plotted separately for the first (A) and last (B) nose pokes in the sequence to show the increase in RT to initiate and decrease in RT to complete repeated sequences. C, D, The effects of repetition across the 10 sessions in which sequence A was repeated. This was measured for individual animals by subtracting mean median RTs for random sessions R1, R2, and R3 (which occurred immediately before, in the middle, and immediately after the 10 sequence A sessions) from median RTs for each session in which sequence A was repeated. Results are plotted separately for the first (C) and last (D) nose pokes in the sequences. E, Median RTs for each response in serial reaction time sequences averaged across sessions in which sequence A was repeated compared with random sessions R1, R2, and R3. Error bars represent SEM.

Figure 8.

Interference effects measured as differences in RT for individual responses in repeated and random serial reaction time sequences. Positive scores indicate longer RTs for random sequences (beneficial effects of repetition). Results are reported for the transition from the fifth session with sequence A to the second random session (A5/R2), the 10th session with sequence A to the third random session (A10/R3), the fifth session with sequence B to the fourth random session (B5/R4), and the average of these three transitions. Error bars represent SEM. For the average scores, significant interference effects (absolute differences >0, two-tailed t test) are indicated by *p < 0.05 or **p < 0.01.