Bethany Plakke

Auditory connections and functions of prefrontal cortex.

The functional auditory system extends from the ears to the frontal lobes with successively more complex functions occurring as one ascends the hierarchy of the nervous system. Several areas of the frontal lobe receive afferents from both early and late auditory processing regions within the temporal lobe. Afferents from the early part of the cortical auditory system, the auditory belt cortex, which are presumed to carry information regarding auditory features of sounds, project to only a few prefrontal regions and are most dense in the ventrolateral prefrontal cortex (VLPFC). In contrast, projections from the parabelt and the rostral superior temporal gyrus (STG) most likely convey more complex information and target a larger, widespread region of the prefrontal cortex. Neuronal responses reflect these anatomical projections as some prefrontal neurons exhibit responses to features in acoustic stimuli, while other neurons display task-related responses. For example, recording studies in non-human primates indicate that VLPFC is responsive to complex sounds including vocalizations and that VLPFC neurons in area 12/47 respond to sounds with similar acoustic morphology. In contrast, neuronal responses during auditory working memory involve a wider region of the prefrontal cortex. In humans, the frontal lobe is involved in auditory detection, discrimination, and working memory. Past research suggests that dorsal and ventral subregions of the prefrontal cortex process different types of information with dorsal cortex processing spatial/visual information and ventral cortex processing non-spatial/auditory information. While this is apparent in the non-human primate and in some neuroimaging studies, most research in humans indicates that specific task conditions, stimuli or previous experience may bias the recruitment of specific prefrontal regions, suggesting a more flexible role for the frontal lobe during auditory cognition.

Metabolic mapping of the rat cerebellum during delay and trace eyeblink conditioning

The essential neural circuitry for delay eyeblink conditioning has been largely identified, whereas much of the neural circuitry for trace conditioning has not been identified. The major difference between delay and trace conditioning is a time gap between the presentation of the conditioned stimulus (CS) and the unconditioned stimulus (US) during trace conditioning. It is this time gap or trace interval which accounts for an additional memory component in trace conditioning. Additional neural structures are also necessary for trace conditioning, including hippocampus and prefrontal cortex. This addition of forebrain structures necessary for trace but not delay conditioning suggests other brain areas become involved when a memory gap is added to the conditioning parameters. A metabolic marker of energy use, radioactively labeled glucose analog, was used to compare differences in glucose analog uptake between delay, trace, and unpaired experimental groups in order to identify new areas of involvement within the cerebellum. Known structures such as the interpositus nucleus and lobule HVI showed increased activation for both delay and trace conditioning compared to unpaired conditioning. However, there was a differential amount of activation between anterior and posterior portions of the interpositus nucleus between delay and trace, respectively. Cerebellar cortical areas including lobules IV and V of anterior lobe, Crus I, Crus II, and paramedian lobule also showed increases in activity for delay conditioning but not for trace conditioning. Delay and trace eyeblink conditioning both resulted in increased metabolic activity within the cerebellum but delay conditioning resulted in more widespread cerebellar cortical activation.

Neural correlates of auditory recognition memory in primate lateral prefrontal cortex

The neural underpinnings of working and recognition memory have traditionally been studied in the visual domain and these studies pinpoint the lateral prefrontal cortex (lPFC) as a primary region for visual memory processing (Miller et al., 1996; Ranganath et al., 2004; Kennerley and Wallis, 2009). Herein, we utilize single-unit recordings for the same region in monkeys (Macaca mulatta) but investigate a second modality examining auditory working and recognition memory during delayed matching-to-sample (DMS) performance. A large portion of neurons in the dorsal and ventral banks of the principal sulcus (area 46, 46/9) show DMS event-related activity to one or more of the following task events: auditory cues, memory delay, decision wait time, response, and/or reward portions. Approximately 50% of the neurons show evidence of auditory-evoked activity during the task and population activity demonstrated encoding of recognition memory in the form of match enhancement. However, neither robust nor sustained delay activity was observed. The neuronal responses during the auditory DMS task are similar in many respects to those found within the visual working memory domain, which supports the hypothesis that the lPFC, particularly area 46, functionally represents key pieces of information for recognition memory inclusive of decision-making, but regardless of modality.

Primate Auditory Recognition Memory Performance Varies With Sound Type

Neural correlates of auditory processing, including for species-specific vocalizations that convey biological and ethological significance (e.g., social status, kinship, environment), have been identified in a wide variety of areas including the temporal and frontal cortices. However, few studies elucidate how non-human primates interact with these vocalization signals when they are challenged by tasks requiring auditory discrimination, recognition and/or memory. The present study employs a delayed matching-to-sample task with auditory stimuli to examine auditory memory performance of rhesus macaques (Macaca mulatta), wherein two sounds are determined to be the same or different. Rhesus macaques seem to have relatively poor short-term memory with auditory stimuli, and we examine if particular sound types are more favorable for memory performance. Experiment 1 suggests memory performance with vocalization sound types (particularly monkey), are significantly better than when using non-vocalization sound types, and male monkeys outperform female monkeys overall. Experiment 2, controlling for number of sound exemplars and presentation pairings across types, replicates Experiment 1, demonstrating better performance or decreased response latencies, depending on trial type, to species-specific monkey vocalizations. The findings cannot be explained by acoustic differences between monkey vocalizations and the other sound types, suggesting the biological, and/or ethological meaning of these sounds are more effective for auditory memory.

Scopolamine impairs auditory delayed matching-to-sample performance in monkeys.

Information concerning the major neurotransmitters critical for auditory memory is sparse. One possibility is the cholinergic system, important for performance in some tasks requiring visual short-term memory and attention [T.G. Aigner, M. Mishkin, The effects of physostigmine and scopolamine on recognition memory in monkeys, Behav. Neural. Biol. 45 (1986) 81-87; N. Hironaka, K. Ando, Effects of cholinergic drugs on scopolamine-induced memory impairment in rhesus monkeys, Jpn. J. Psychopharmacol. 16 (1996) 103-108; T.M. Myers, G. Galbicka, M.L. Sipos, S. Varadi, J.L. Oubre, M.G. Clark, Effects of anticholinergics on serial-probe recognition accuracy of rhesus macaques (Macaca mulatta), Pharmacol. Biochem. Behav. 73 (2002) 829-834; H. Ogura, T.G. Aigner, MK-801 Impairs recognition memory in rhesus monkeys: comparison with cholinergic drugs, J. Pharmacol. Exp. Ther. 266 (1993) 60-64; D.M. Penetar, J.H. McDonough Jr., Effects of cholinergic drugs on delayed match-to-sample performance of rhesus monkeys, Pharmacol. Biochem. Behav. 19 (1983) 963-967; M.A. Taffe, M.R. Weed, L.H. Gold, Scopolamine alters rhesus monkey performance on a novel neuropsychological test battery, Cogn. Brain Res. 8 (1999) 203-212]. Five rhesus monkeys were trained to perform an auditory go/no-go delayed matching-to-sample (DMTS) task wherein two acoustic stimuli (500ms), separated by variable memory delays (500ms, 2500ms, or 5000ms), were either identical sound presentations, i.e., match trials, or two different sound presentations, i.e., nonmatch trials. Sound stimuli were chosen semi-randomly from a large set sound set ( approximately 900). After reaching a criterion of 80% correct on the behavioral task, monkeys were injected with saline or doses of scopolamine hydrochloride mixed in saline (3 microg, 5 microg, and 10 microg per 1kg of weight), 30 min before training. Scopolamine impaired performance accuracy on match trials in a dose-dependent manner. Blocking muscarinic receptors with scopolamine did not significantly impair motor responses, food motivation, or responses to rewarded sound. These findings support the hypothesis that the cholinergic system is important for auditory short-term memory.

Metabolic mapping of rat forebrain and midbrain during delay and trace eyeblink conditioning

While the essential neural circuitry for delay eyeblink conditioning has been largely identified, much of the neural circuitry for trace conditioning has yet to be determined. The major difference between delay and trace conditioning is a time gap between the presentation of the conditioned stimulus (CS) and the unconditioned stimulus (US) during trace conditioning. It is this time gap, which accounts for the additional memory component and may require extra neural structures, including hippocampus and prefrontal cortex. A metabolic marker of energy use, radioactively labeled glucose analog, was used to compare differences in glucose analog uptake between delay, trace, and unpaired experimental groups (rats, Long-Evans), to identify possible new areas of involvement within forebrain and midbrain. Here, we identify increased 2-DG uptake for the delay group compared to the unpaired group in various areas including: the medial geniculate nuclei (MGN), the amygdala, cingulate cortex, auditory cortex, medial dorsal thalamus, and frontal cortices. For the trace group, compared to the unpaired group, there was an increase in 2-DG uptake for the medial orbital frontal cortex and the medial MGN. The trace group also exhibited more increases lateralized to the right hemisphere, opposite to the side of US delivery, in various areas including: CA1, subiculum, presubiculum, perirhinal cortex, ventral and dorsal MGN, and the basolateral and central amygdala. While some of these areas have been identified as important for delay or trace conditioning, some new structures have been identified such as the orbital frontal cortex for both delay and trace groups.

Neural circuits in auditory and audiovisual memory

Working memory is the ability to employ recently seen or heard stimuli and apply them to changing cognitive context. Although much is known about language processing and visual working memory, the neurobiological basis of auditory working memory is less clear. Historically, part of the problem has been the difficulty in obtaining a robust animal model to study auditory short-term memory. In recent years there has been neurophysiological and lesion studies indicating a cortical network involving both temporal and frontal cortices. Studies specifically targeting the role of the prefrontal cortex (PFC) in auditory working memory have suggested that dorsal and ventral prefrontal regions perform different roles during the processing of auditory mnemonic information, with the dorsolateral PFC performing similar functions for both auditory and visual working memory. In contrast, the ventrolateral PFC (VLPFC), which contains cells that respond robustly to auditory stimuli and that process both face and vocal stimuli may be an essential locus for both auditory and audiovisual working memory. These findings suggest a critical role for the VLPFC in the processing, integrating, and retaining of communication information. This article is part of a Special Issue entitled SI: Auditory working memory.