Specific long-term memory traces in primary auditory cortex

Abstract

Learning and memory involve the storage of specific sensory experiences. However, until recently the idea that the primary sensory cortices could store specific memory traces had received little attention. Converging evidence obtained using techniques from sensory physiology and the neurobiology of learning and memory supports the idea that the primary auditory cortex acquires and retains specific memory traces about the behavioural significance of selected sounds. The cholinergic system of the nucleus basalis, when properly engaged, is sufficient to induce both specific memory traces and specific behavioural memory. A contemporary view of the primary auditory cortex should incorporate its mnemonic and other cognitive functions.Identifying the neural substrates of learning and memory is a core problem in neuroscience. As memories involve the representation of past sensory events, they may be stored, in part, within sensory systems. Sensory systems have traditionally been viewed as 'stimulus analysers', with learning and memory assigned to 'higher' cortical regions. Nonetheless, neurophysiological studies have produced evidence for learning-induced plasticity in sensory cortices, and in particular the auditory cortex. Galambos and colleagues first implicated the primary auditory cortex (A1) in learning in 1956, observing that pairing an auditory conditioned stimulus (CS) with a weak shock (a mildly aversive unconditioned stimulus (US)) produced a significant increase in the amplitude of CS-elicited evoked field potentials in A1 of the cat 1 . Subsequently, these findings were extended to other tasks (such as discrimination), types of learning (including instrumental conditioning), motivations (for example, food) and types of recording (such as single and multiple unit discharges) 2 .Although such results established associative plasticity in A1, neither they nor similar findings in other sensory cortices addressed the key issue of specificity of information storage. As memories have specific content, how could changes in the magnitude of sensory cortical responses adequately reflect the encoding of specific aspects of experiences? A solution was provided by the field of sensory neurophysiology, which focuses on stimulus specificity. Sensory physiology experiments use a wide range of stimulus values to NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript determine how specific sensory stimuli are processed and coded. In fact, the basic paradigms of sensory physiology and learning are complementary (Box 1).This article presents an overview of research that combines experimental designs from sensory physiology with those of learning and memory to search for specific memory traces in A1. A sign of a specific memory trace would be learning-induced physiological plasticity that has the key characteristics of behavioural memory and sufficient specificity to encode a canonical attribute of experience, such as a physical feature and its behavioural importance. Previous reviews have covered ot...

NMDA-dependent facilitation of corticostriatal plasticity by the amygdala

“…Although many studies have examined how the BLA facilitates synaptic plasticity in its targets, their relevance to corticostriatal plasticity is unclear. For instance, one model centers on the ability of the BLA to recruit corticopetal basal forebrain cholinergic neurons (48). This BLA-driven release of acetylcholine would facilitate plasticity in cortical networks.…”

A synaptic memory trace for cortical receptive field plasticity

“…How do the synaptic modifications observed here correspond to previously reported changes in excitability 17,22 and spike generation 4,9,19 ? To determine the relation between changes in synaptic input and spike output, we made current-clamp recordings from AI neurons to measure tone-evoked spiking responses before and after NB pairing.…”

“…5b). Thus NB pairing alters the firing mode of cortical neurons, increasing the output of AI to enhance the salience of particular stimuli such as those with new behavioral relevance 4,9,18 or during periods of increased perceptual demand on attention 15,30 .…”

“…Neuromodulation is required for cortical plasticity, but it is uncertain how subcortical neuromodulatory systems, such as the cholinergic nucleus basalis ( A major subcortical nucleus critical for receptive field plasticity is NB, the main source of cortical acetylcholine (ACh) 4,9,[14][15][16][17][19][20][21] . How are neuromodulators such as ACh involved in plasticity, and what circuit elements do they act upon?…”

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).…”