Abstract
The ability to inhibit action is critical for everyday behavior and is affected by a variety of disorders. Behavioral control and response inhibition is thought to depend on a neural circuit that includes the dorsal striatum, yet the neural signals that lead to response inhibition and its failure are unclear. To address this issue, we recorded from neurons in rat dorsomedial striatum (mDS) in a novel task in which rats responded to a spatial cue that signaled that reward would be delivered either to the left or to the right. On 80% of trials rats were instructed to respond in the direction cued by the light (GO). On 20% of trials a second light illuminated instructing the rat to refrain from making the cued movement and move in the opposite direction (STOP). Many neurons in mDS encoded direction, firing more or less strongly for GO movements made ipsilateral or contralateral to the recording electrode. Neurons that fired more strongly for contralateral GO responses were more active when rats were faster, showed reduced activity on STOP trials, and miscoded direction on errors, suggesting that when these neurons were overly active, response inhibition failed. Neurons that decreased firing for contralateral movement were excited during trials in which the rat was required to stop the ipsilateral movement. For these neurons activity was reduced when errors were made and was negatively correlated with movement time suggesting that when these neurons were less active on STOP trials, response inhibition failed. Finally, the activity of a significant number of neurons represented a global inhibitory signal, firing more strongly during response inhibition regardless of response direction. Breakdown by cell type suggests that putative medium spiny neurons (MSNs) tended to fire more strongly under STOP trials, whereas putative interneurons exhibited both activity patterns.
Highlights
Dorsal striatum has been implicated in habitual, over-learned, and automatic behaviors (Miyachi et al, 1997; Jog et al, 1999; Matsumoto et al, 1999; Graybiel, 2000; Bailey and Mair, 2006; Yin and Knowlton, 2006; Schmitzer-Torbert and Redish, 2008), recent work has pointed to the mDS as being part of a circuit that is involved in response inhibition (Eagle and Baunez, 2010)
We found signals related to response inhibition and the miscoding of direction on STOP trials in which rats had to cancel movement and redirect behavior
We designed a novel task that allowed us to examine neural activity when rats had to inhibit a response that occurred on the large majority of trials and redirect behavior toward the opposite location
Summary
The ability to inhibit action is critical for everyday behavior and is disrupted in several diseases including attention deficit hyperactivity disorder, schizophrenia, substance abuse, pathological gambling, Tourette syndrome, Parkinson’s Disease, and obsessive-compulsive disorder (Schachar et al, 1995; Oosterlaan and Sergeant, 1998; Oosterlaan et al, 1998; Rubia et al, 1998, 2005, 2007; Fillmore and Rush, 2002; Gauggel et al, 2004; Aron and Poldrack, 2005; Kalanithi et al, 2005; Monterosso et al, 2005; Nigg et al, 2005; Bellgrove et al, 2006; Fillmore et al, 2006; Schachar et al, 2007; Durston et al, 2009; Eagle and Baunez, 2010; Kataoka et al, 2010; Leventhal et al, 2012). Responses made prior to the end the delay period were considered premature errors and were more common in rats with DS lesions This result suggests that response inhibition is dependent on DS, others have failed to report premature responding after DS lesions during performance of similar tasks (Brown and Robbins, 1989; Hauber and Schmidt, 1994; Eagle and Baunez, 2010). To better understand what goes wrong in disorders that impact impulse control, we first need to elucidate what neural signals give rise to behavior To address these issues we devised a modified version of tasks commonly used in clinical studies to assess the ability to stop an ongoing action. We found signals related to response inhibition and the miscoding of direction on STOP trials in which rats had to cancel movement and redirect behavior
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