Scientific Understanding of Consciousness
Consciousness as an Emergent Property of Thalamocortical Activity

Emotional Memory Storage — Secondary Sensory Cortices



Science 6 August 2010: Vol. 329. no. 5992, pp. 649 - 656

Role of Secondary Sensory Cortices in Emotional Memory Storage and Retrieval in Rats

Tiziana Sacco1 and Benedetto Sacchetti1,2

1 Department of Neuroscience, University of Turin, Corso Raffaello 30, I-10125 Turin, Italy.
2 National Institute of Neuroscience, I-10125 Turin, Italy.


Visual, acoustic, and olfactory stimuli associated with a highly charged emotional situation take on the affective qualities of that situation. Where the emotional meaning of a given sensory experience is stored is a matter of debate. We found that excitotoxic lesions of auditory, visual, or olfactory secondary sensory cortices impaired remote, but not recent, fear memories in rats. Amnesia was modality-specific and not due to an interference with sensory or emotional processes. In these sites, memory persistence was dependent on ongoing protein kinase M{zeta} activity and was associated with an increased activity of layers II–IV, thus suggesting a synaptic strengthening of corticocortical connections. Lesions of the same areas left intact the memory of sensory stimuli not associated with any emotional charge. We propose that secondary sensory cortices support memory storage and retrieval of sensory stimuli that have acquired a behavioral salience with the experience.

During an emotional experience, sensory stimuli such as odors, sounds, and colors are associated with the affective qualities of that situation. Despite recent advances, the question of how and where the brain stores permanent emotional memories remains elusive. Because memories involve the representation of past sensory and emotional events, they may be stored, in part, within the sensory cortex. Nonetheless, lesions of sensory cortices do not prevent the formation of emotional memories. However, such lesions have been performed before or shortly after learning, a time interval in which thalamus-amygdala circuits support the functional absence of sensory cortices. No data are available on the involvement of the sensory cortex in long-term storage and retrieval of emotional memories. Therefore, we addressed two related questions: Are sensory cortices necessary for the storage and retrieval of remote fear memories? And if so, what is the role played by these sites?

The primary auditory cortex is surrounded by a belt region that constitutes the secondary auditory area. We therefore examined whether the secondary auditory cortex participates in remote fear memory storage and retrieval.

Collectively, the results indicate that each secondary sensory cortex is involved in emotional memories related to a specific sensory modality. The modality-specific involvement of sensory cortices suggests that lesions of these sites do not affect innate fear behavior.

As fear memories mature, they become dependent on sensory cortices. Because previous and present results also support a role for the amygdala in the retrieval of remote memories, it may be that permanent memories are widely distributed across sensory cortices and amygdala neurons (as well as other sites). However, because of its anatomical and functional connections, the amygdala may provide the necessary link between neural sites that encode memory and autonomic or motor effectors. Our data do not allow us to discriminate between these possibilities; they indicate only that the amygdala alone is not sufficient to support permanent fear memories.

The anterior cingulate cortex also participates in the storage of permanent fear memories. This site plays an integrative role in emotional and cognitive control processes (e.g., attention, error detection and correction). In addition, it may also encode information about the aversive components of an emotional experience. Indeed, it may interact with sensory cortices to provide the integration among the multiple representations occurring in sensory cortices during memory storage.

Both previous and present data support the view that secondary cortices encode the emotional valence acquired by sensory stimuli with the experience. Previous findings have shown that plasticity related to long-term acoustic habituation takes place in the lower auditory system (i.e., brainstem and auditory nuclei) but not in the auditory cortex, and that olfactory long-term habituation is related to olfactory bulb activity

Secondary cortices that perform high-level sensory analysis combine sensory processing and memory plasticity to encode the behavioral salience of perceiving stimuli. Such information becomes widely distributed throughout the cortex, each secondary sensory cortex coding the valence of stimuli of a specific modality. Such a memory storage mechanism results in a synaptic strengthening of corticocortical connections that may provide the integrated view of the whole emotional experience during memory recall.

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