The hearing hippocampus

Abstract

The hippocampus has a well-established role in spatial and episodic memory but a broader function has been proposed including aspects of perception and relational processing. Neural bases of sound analysis have been described in the pathway to auditory cortex, but wider networks supporting auditory cognition are still being established. We review what is known about the role of the hippocampus in processing auditory information, and how the hippocampus itself is shaped by sound. In examining imaging, recording, and lesion studies in species from rodents to humans, we uncover a hierarchy of hippocampal responses to sound including during passive exposure, active listening, and the learning of associations between sounds and other stimuli. We describe how the hippocampus' connectivity and computational architecture allow it to track and manipulate auditory information – whether in the form of speech, music, or environmental, emotional, or phantom sounds. Functional and structural correlates of auditory experience are also identified. The extent of auditory-hippocampal interactions is consistent with the view that the hippocampus makes broad contributions to perception and cognition, beyond spatial and episodic memory. More deeply understanding these interactions may unlock applications including entraining hippocampal rhythms to support cognition, and intervening in links between hearing loss and dementia.

Hippocampal atrophy is associated with hearing loss in cognitively normal adults

“…The hippocampus plays a multifaceted role in information processing and memory, with the right hippocampus generally implicated in spatial navigation and visual memory, while the left hippocampus predominantly engages in perception, learning and recall of speech (Ezzati et al, 2016;Billig et al, 2022). Our results specifically implicate the left hippocampus, consistent with its known lateralization.…”

“…Our results specifically implicate the left hippocampus, consistent with its known lateralization. The hippocampus certainly receives and operates on auditory information (for a review, see Billig et al, 2022), and its pyramidal place cells (O' Keefe and Dostrovsky, 1971) can map out dimensions of sound as they do for space, at least in rodents (Aronov et al, 2017). The hippocampus is also active during auditory working memory (Bishop and Miller, 2009;Davis et al, 2011;Kumar et al, 2016;Lad et al, 2020;Kumar et al, 2021) and may provide predictive information to superior temporal sites during continuous speech listening (Michelmann et al, 2021).…”

Altered auditory processes pattern predicts cognitive decline in older adults: different modalities with aging

“…There are several possible mechanisms for the relationship between hearing impairment and cognitive impairment: common pathology, impoverished input, occupation of cognitive resources and functionpathology interaction (Griffiths et al, 2020). A recent review highlighted the interaction of auditory processing with the hippocampus and the possible outcome on cognition (Billig et al, 2022). Moderate noise exposure in rats specifically impaired neuroplasticity in the hippocampus and cerebral cortex which led to deleterious cognitive outcomes, and a study in gorillas found that a deficit of auditory processes was associated with damage in the integrity of white matter in hippocampus-related structures, leading to extensive cognitive compromise (Gray et al, 2020;Zhang et al, 2021).…”

Sensory Loss and Risk of Dementia

“…There is a growing body of literature that the medial temporal lobe including the hippocampus, key brain structures implicated in AD, is involved in auditory processing ( Billig and others 2022 ). Human functional imaging studies demonstrate the involvement of these structures in real-world listening under adverse conditions, such as speech-in-noise perception ( Griffiths and others 2020 ).…”

“…Human functional imaging studies demonstrate the involvement of these structures in real-world listening under adverse conditions, such as speech-in-noise perception ( Griffiths and others 2020 ). Auditory cognition relevant to real-world listening, including working memory for sounds, has been shown to depend on hippocampal mechanisms ( Billig and others 2022 ). Rodent work supports specific roles for medial temporal lobe structures in auditory cognition: Aronov and others (2017) demonstrated that single units in the hippocampus were tuned to specific frequencies during a working memory task, consistent with the use of hippocampal computational mechanisms for auditory analysis.…”