Dorsolateral striatum is critical for the expression of surprise‐induced enhancements in cue associability

Abstract

The dorsolateral striatum (DLS) is frequently implicated in sensory-motor integration, including the performance of sensory orienting responses and learned stimulus-response habits. Our laboratory previously identified a role for the DLS in rats' performance of conditioned orienting responses (ORs) to Pavlovian cues for food delivery. Here, we considered whether DLS is also critical to another aspect of attention in associative learning, the surprise-induced enhancement of cue associability. A large behavioral literature shows that a cue present when an expected event is omitted enters into new associations more rapidly, when that cue is subsequently paired with food. Research from our laboratory has shown that both cue associability enhancements and conditioned ORs depend on the function of a circuit that includes the amygdala central nucleus and the substantia nigra pars compacta. In three experiments, we explored the involvement of DLS in surprise-induced associability enhancements, using a three-stage serial prediction task that permitted separation of DLS function in registering surprise (prediction error) and enhancing cue associability, and in using that increased associability to learn more rapidly about that cue later. The results showed that DLS is critical to the expression, but not the establishment, of the enhanced cue associability normally produced by surprise in this task. They extend the role of DLS and the amygdalo-nigro-striatal circuit underlying learned orienting to more subtle aspects of attention in associative learning, but are consistent with the general notion that DLS is more important in the expression of previously-acquired tendencies than in their acquisition.

Amygdalo-striatal interaction in the enhancement of stimulus salience in associative learning.

“…It is tempting to suggest that DLS may serve as a common path for expression of many examples of enhanced processing of sensory cues. Our data (together with those of Asem et al, 2014) suggest that expression of associability changes may require convergence of enhanced associability produced and encoded elsewhere (e.g., Schiffino et al, 2014) with enhanced sensory drive provided by DLS processing.…”

“…Recently, we found that bilateral lesions of the DLS eliminated surprise-induced cue salience enhancements in a serial prediction task (Asem et al, 2014) that was previously shown to require intact CeA function (Holland & Gallagher, 1993a; 2006). Although the observation that bilateral disruption of CeA or DLS prevents salience enhancements could suggest that those regions are part of the same, serial circuit, it is possible that striatal influences act independently of the CeA circuit previously studied.…”

Mini-review: Prediction errors, attention and associative learning

“…Comparable lesion experiments identified a number of brain regions as critical to the display of a shift advantage in this task, including substantia nigra pars compacta (SNc, Lee et al, 2006), substantia innominata/nucleus basalis magnocellularis (SI; Chiba et al, 1995) and its cholinergic afferentation of the posterior parietal cortex (PPC; Bucci et al, 1998), the dorsolateral striatum (DLS; Asem et al, 2015), the lateral hypothalamus (LH; Wheeler et al, 2014), and portions of the medial prefrontal cortex (Maddux, 2008). As with CeA lesions, none of these manipulations affected losses in cue associability in the consistent condition.…”

“…There was no evidence that either structure was involved in reductions in associability: the rats in the consistent groups all learned at the same rate. Subsequent experiments of this type suggest the SNc (Lee et al, 2008) to be within the surprise module only, and the secondary visual cortex (SVC; Schiffino, 2015; Schiffino & Holland, 2016b) and the DLS (Asem et al, 2015) as participating in the expression module only. We found only one region, the PPC, critical to both the surprise and expression modules (Schiffino et al, 2014a).…”

Consolidation of altered associability information by amygdala central nucleus

“…Both the CeA (Holland & Gallagher, 2006) and its interactions with the substantia nigra pars compacta (SNc; Lee et al, 2006, 2008) are critical at the time of surprise but not at the time of expression of enhanced cue associability in test, whereas the cholinergic substantia innominata/nucleus basalis magnocellularis (SI/nBm; Holland & Gallagher, 2006), dorsolateral striatum (Asem et al, 2015), and secondary visual cortex (Schiffino & Holland, 2016) are critical at the time of expression, but not at the time of surprise.…”