Anatomical pathways for auditory memory II: information from rostral superior temporal gyrus to dorsolateral temporal pole and medial temporal cortex

Abstract

Auditory recognition memory in non-human primates differs from recognition memory in other sensory systems. Monkeys learn the rule for visual and tactile delayed matching-to-sample within a few sessions, and then show one-trial recognition memory lasting 10–20 min. In contrast, monkeys require hundreds of sessions to master the rule for auditory recognition, and then show retention lasting no longer than 30–40 s. Moreover, unlike the severe effects of rhinal lesions on visual memory, such lesions have no effect on the monkeys' auditory memory performance. The anatomical pathways for auditory memory may differ from those in vision. Long-term visual recognition memory requires anatomical connections from the visual association area TE with areas 35 and 36 of the perirhinal cortex (PRC). We examined whether there is a similar anatomical route for auditory processing, or that poor auditory recognition memory may reflect the lack of such a pathway. Our hypothesis is that an auditory pathway for recognition memory originates in the higher order processing areas of the rostral superior temporal gyrus (rSTG), and then connects via the dorsolateral temporal pole to access the rhinal cortex of the medial temporal lobe. To test this, we placed retrograde (3% FB and 2% DY) and anterograde (10% BDA 10,000 mW) tracer injections in rSTG and the dorsolateral area 38DL of the temporal pole. Results showed that area 38DL receives dense projections from auditory association areas Ts1, TAa, TPO of the rSTG, from the rostral parabelt and, to a lesser extent, from areas Ts2-3 and PGa. In turn, area 38DL projects densely to area 35 of PRC, entorhinal cortex (EC), and to areas TH/TF of the posterior parahippocampal cortex. Significantly, this projection avoids most of area 36r/c of PRC. This anatomical arrangement may contribute to our understanding of the poor auditory memory of rhesus monkeys.

Functional connectivity based parcellation of the human medial temporal lobe

“…Alternatively, it is possible that an “item” is separately and differentially processed by antPRC and postPRC might, with postPRC preferentially emphasizing visual properties and antPRC preferentially emphasizing auditory properties, personal significance, and relevance for action selection (Belin et al 2000; Belin at al. 2002; Olson et al, 2007; Petkov et al 2008; Munoz-Lopez et al, 2015). These ideas are of course speculative, and further research is needed to better understand how the antPRC, postPRC, and PHC separately and collectively encode the attributes of an event.…”

Auditory short-term memory in the primate auditory cortex

“…Recent evidence shows that human auditory memory is inferior to visual memory, whether for colors and tones in STM or complex objects in LTM (Bigelow and Poremba, 2014; see also Cohen et al, 2009). Connectional neuroanatomy in the monkey reveals an impoverished pathway from the auditory cortex to the medial temporal lobe, which may underlie the relative difficulty of forming and recalling auditory memories relative to visual memories (Munoz-Lopez et al, 2010; Munoz-Lopez et al, 2015). The homology between auditory memory pathways in the human and nonhuman primate is a critical open question, but both species may be operating under similar constraints.…”

“…A possible anatomical correlate of this inability lies in the paucity of auditory inputs to the MTL, which receives sensory input predominantly from higher visual cortex (Munoz-Lopez et al, 2010; Munoz-Lopez et al, 2015; Suzuki and Amaral, 1994). As the MTL is necessary for the formation of long-term visual memories (Mishkin, 1978), purely auditory stimuli may not have direct access to this mechanism of storage.…”

Auditory object perception: A neurobiological model and prospective review

“…However, hearing is different, both in terms of the physical signal attribute differences that need to be reconstructed by the brain, but more so the level of spectro-temporal discrimination that evolved in hominins (see glossary). Out of survival necessity, and now unique to humans, the auditory-vocal system had evolved the ability to convey and interpret increasingly subtle socially relevant emotional states of others (Donald, 1991; Munoz-Lopez et al, 2015; Fritz et al, 2016). Moreover, the formalization and unification of thought and knowledge in cortex is thought to have set the stage for spoken language systems to develop together with vastly greater degrees of auditory working memory abilities.…”