Associations and Rewards in the Auditory Cortex
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In psychology, the term association refers to a connection between different elementary mental entities (sensations, thoughts, feelings; Dudai 2002). Aside from innate, reflex-like associations, novel associations are typically acquired during learning. In Pavlovian/classical conditioning, a stimulus-stimulus association is formed by repetitively pairing an initially neutral stimulus with a biologically significant unconditioned stimulus that automatically triggers an unconditioned behavioral response. In instrumental/operant conditioning, a stimulus-response association is formed in the presence of reinforcers. Reinforcers can be either positive, such as water, food, money, and brain stimulation reward, and result in an increase in the probability of a response to the stimulus. Negative reinforcers (e.g., footshocks, airpuffs, money loss) decrease the probability of a response to the stimulus. If the reinforcer is removed, the learned associations risk extinction.
Classical View of Brain Structures Reflecting Associations and Reinforcement
Traditionally associative functions are assigned to the so-called association cortex (Creutzfeldt 1983). Inspired by “associationism” (the philosophical doctrine that the mind learns and construes the world bottom up by associating mental entities) and based on anatomical considerations, Flechsig originally defined the association cortex as that part of the cerebral cortex that appeared to lack direct afferences from the senses and efferences to peripheral motor structures. He proposed that the association cortex provides the substrate for the fusion of primary sensations to obtain ideas of objects as a whole. This idea is challenged, inter alia, by studies demonstrating associative functions already in primary sensory cortices, which have direct afferences from the senses. In addition, the sensory cortex is affected by reinforcement (Shuler and Bear 2006; Brosch et al. 2011a; Arsenault et al. 2013; Weis et al. 2013), which generally is thought to involve the limbic system, including the hypothalamus, amygdala, hippocampus, septal nuclei, ventral tegmental area, and anterior cingulate gyrus. These findings put into question the existence of unisensory cortical areas at all (Ghazanfar and Schroeder 2006).
Learning associations between stimuli, between stimuli and behavioral responses, or between stimuli and reinforcers change the auditory cortex, such as the feature sensitivity (spectrotemporal receptive field) of neurons in the auditory cortex, their response strength and response latency, as well as interneuronal synchrony (Scheich and Brosch 2013; Shepard et al. 2013). In detection tasks, the direction of the receptive field change at the frequency of the conditioned tone depends on the valence of the tone (Scheich et al. 2011); if it is negative (associated with punishment), the response to the tone is increased (receptive field is sensitized at the conditioned tone frequency); if it is positive (associated with reward), the response is decreased (receptive field is suppressed at the conditioned tone frequency). In frequency discrimination tasks, slopes of spectral tuning curves become sharper around the conditioned frequencies. In categorization tasks, stimuli of the same category evoke (spatiotemporal) neuronal activity patterns that are more similar to each other than those evoked by stimuli of other categories.
These changes coincide with or may even form the basis of changes in representation maps (e.g., tonotopic frequency map) in the auditory cortex that occur, at least transiently, after learning (Shepard et al. 2013; Grosso et al. 2015). They may also underlie plasticity of neuronal mass activity, as revealed by electro- and magnetoencephalography (EEG, MEG) or functional magnetic resonance imaging (fMRI) (Rüsseler et al. 2005).
The formation of novel associations in the auditory cortex requires the involvement of neuromodulators (Shepard et al. 2013). Some of the described changes can also be mimicked by repetitively pairing auditory stimuli with electrical stimulation of neuromodulatory systems, such as the ventral tegmental area (dopamine; Huang et al. 2016a), the nucleus basalis of Meynert (acetylcholine; Bakin and Weinberger 1996), the locus coeruleus (norepinephrine; Martins and Froemke 2015), or the vagus nerve (triggering widespread release of neuromodulators; Engineer et al. 2011). Formation of associations in the auditory cortex also involves cognitive factors: changes in the auditory cortex and learning do not occur when an animal is passively exposed to the stimulus-reward pairings of another animal while it was instrumentally conditioned (Blake et al. 2006).
Neuronal Correlates of Association
Sustained firing and slow firing changes may provide neuronal correlates of associations between mental entities (Brosch et al. 2011a). The main condition necessary for the emergence of slow firing changes is that subjects have learnt that conditioned associations are contingent on reinforcers. When the reinforcer is removed, the slow firing changes disappear within a few trials, concomitantly with behavioral changes (Huang et al. 2016b). These firings may be related to the contingent negative variation (Walter et al. 1964), an event-related potential that can be obtained in electroencephalography in humans. It is considered to reflect the contingency and the contiguity of two events that have a motivational “value.”
Different types of events may be associated through event-related slow firing changes (Brosch et al. 2011a). Events that trigger such changes can be auditory (and possibly visual) stimuli, reinforcers, and behavioral responses, like grasping. An event with which slow firing changes end is the reinforcer. Slow firing changes have been observed between (1) an auditory stimulus and a reinforcer, (2) a behavioral response and an auditory stimulus, and (3) a behavioral response and another behavioral response.
The association between behaviorally significant events provided by slow firing changes might even be directed in some cases, that is, this type of firing might provide some sort of either prospective coding of an upcoming event or retrospective coding about a preceding event.
Neuronal Correlates of Rewards
In animals actively engaged in listening to auditory stimuli, direct reflections of rewards have been demonstrated in the auditory cortex. Neuronal activity in the auditory cortex varied with the size of the delivered reward and the size of the reward that was expected to be earned in a future auditory task, as well as the magnitude of the mismatch between the expected and delivered reward (the reward prediction error) (Brosch et al. 2011b). Reflections of rewards are also present in other sensory cortices (Shuler and Bear 2006; Arsenault et al. 2013).
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