Associative representational plasticity in the auditory cortex: A synthesis of two disciplines

Abstract

Historically, sensory systems have been largely ignored as potential loci of information storage in the neurobiology of learning and memory. They continued to be relegated to the role of "sensory analyzers" despite consistent findings of associatively induced enhancement of responses in primary sensory cortices to behaviorally important signal stimuli, such as conditioned stimuli (CS), during classical conditioning. This disregard may have been promoted by the fact that the brain was interrogated using only one or two stimuli, e.g., a CS + sometimes with a CS -, providing little insight into the specificity of neural plasticity. This review describes a novel approach that synthesizes the basic experimental designs of the experimental psychology of learning with that of sensory neurophysiology. By probing the brain with a large stimulus set before and after learning, this unified method has revealed that associative processes produce highly specific changes in the receptive fields of cells in the primary auditory cortex (A1). This associative representational plasticity (ARP) selectively facilitates responses to tonal CSs at the expense of other frequencies, producing tuning shifts toward and to the CS and expanded representation of CS frequencies in the tonotopic map of A1. ARPs have the major characteristics of associative memory: They are highly specific, discriminative, rapidly acquired, exhibit consolidation over hours and days, and can be retained indefinitely. Evidence to date suggests that ARPs encode the level of acquired behavioral importance of stimuli. The nucleus basalis cholinergic system is sufficient both for the induction of ARPs and the induction of specific auditory memory. Investigation of ARPs has attracted workers with diverse backgrounds, often resulting in behavioral approaches that yield data that are difficult to interpret. The advantages of studying associative representational plasticity are emphasized, as is the need for greater behavioral sophistication.

Plasticity of human auditory-evoked fields induced by shock conditioning and contingency reversal

“…This effect might appear potentially consistent with the extensive animal literature on increased representation of CS + within auditory cortex (reviewed in refs. [4][5][6], although some of the single-cell findings from invasive animal recordings were at shorter latencies than the human N1m or P2m (e.g., refs. 1-3).…”

“…[4][5][6] in showing plasticity of auditory cortex responses in animals, when sounds are paired with shock in a classical contingency. However, our findings go beyond previous observations in showing that different hierarchical levels of cortical auditory responses (P1m, N1m, and P2m) are subject to very different constraints in flexibility when faced with a sudden contingency reversal.…”

“…1-3; reviewed in refs. [4][5][6]. Such plasticity can emerge rapidly, persist, and relate to neuromodulation.…”

Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain

“…Furthermore, a substantial amount of experimental data in animals, including primates, suggest the involvement of the basal forebrain in attention, learning, memory, reward and cortical plasticity (Wilson and Rolls, 1990;Richardson and DeLong, 1991;Woytko et al, 1994;Chiba et al, 1995;Everitt and Robbins, 1997;Wang et al, 1997;Gaffan et al, 2002;Muir et al, 2004;Conner et al, 2005;Turchi et al, 2005;Sarter et al, 2006;McGaughy et al, 2006;Weinberger 2007). Similarly, imaging studies in humans -as detailed below -lend support for a role of the basal forebrain in a range of cognitive functions.…”

Region- and Layer-Specific Activation of the Higher Order Auditory Cortex Te2 after Remote Retrieval of Fear or Appetitive Memories

“…From the seminal studies of Scheich and colleagues (Brosch et al 2011;Ohl and Scheich 2005) and Weinberger and colleagues (Weinberger 2004(Weinberger , 2007(Weinberger , 2015, it is becoming clearer that sensory cortices, such as the auditory cortex, participate in the formation and maintenance of emotional memories, and that the role played by these structures in emotional memory goes beyond simple sensory stimuli perception and memorization (reviewed in Fritz et al 2007;Grosso et al 2015a;Shamma and Fritz 2014;Weinberger 2004Weinberger , 2007Weinberger , 2015. In support of this notion, we have identified higher order components of sensory cortices, such as the temporal auditory cortex Te2, which are essential for storing remote fearful memories (Cambiaghi et al 2015;Grosso et al 2015b;Sacco and Sacchetti 2010).…”