Monkeys were trained on an auditory version of delayed matching-to-sample with randomly varying delays of 2-50 sec and retested after being given different types of bilateral temporal lobe lesions. Monkeys that received complete medial temporal removals or removal of only the rostral third of the superior temporal gyrus (STG) were severely impaired even at the shortest delays; whereas those given lesions limited to the rhinal (i.e. perirhinal/entorhinal) cortices, which are known to produce severe impairment in both visual and tactile recognition, were unaffected even at the longest delays. Our results suggest that the critical neural substrates for recognition in the auditory and visual modalities maybe anatomically distinct within the temporal lobe. The deficit in auditory recognition following medial temporal lesions may be due to a disconnection between the STG and other critical areas for memory function located outside the temporal lobe. To identify all the regions, both inside and outside the temporal lobe, that might participate in auditory processing, those regions activated during passive listening to a variety of auditory stimuli were mapped using 2-deoxyglucose autoradiography. The activated regions were found to include the entire extent of the superior temporal gyrus (STG), from its caudal tip to the temporal pole, the parahippocampal gyrus, and many extratemporal areas in the posterior parietal, insular, and prefrontal cortices. Our recent anatomical study shows that the auditory regions in prefrontal cortex receive strong projections from the STG (Romanski et al., Nature Neuroscience 2: 1131-6, 1999). Furthermore, we now have anatomical evidence that medial temporal lobe resections dramatically decrease the auditory pathway from the rostral STG to areas 10,14,24, 32, and 25 of the medial prefrontal cortex and to the medial dorsal nucleus of the thalamus. These results strengthen the hypothesis that a disconnection between STG and prefrontal regions may account for the deficit in auditory recognition memory following medial temporal lesions. An important aspect of auditory processing is the spectral and temporal integration of acoustic information. To examine spectrotemporal integration in the primary auditory cortex of an awake rhesus monkey, we recorded neuronal responses to (a) pure tones and bandpassed noise in order to obtain frequency tuning curves (FTCs), (b) ripple stimuli in order to generate spectrotemporal receptive fields (STRFs), and (c) linear frequency modulated (FM) stimuli, which are natural components of monkey calls. In addition to the typical phasic onset responses observed in the anesthetized animal, primary cortical neurons in the awake monkey showed a variety of temporally structured types of response, including tonic, pauser, and offset responses, which appear to have different distributions in the two primary auditory areas, A1 and R. We also found evidence for greater spectral integration in primary auditory cortex than has previously been described in the anesthetized monkey. Although most of the neurons in the primary auditory cortex respond preferentially to a single best frequency, some neurons (10-15%) show multiple tuning peaks both in their FTCs and STRFs, suggesting that these neurons integrate spectral information over a wide range of frequencies, which is likely to be important in mediating auditory pattern recognition. Also, 75% of A1 and R neurons were selective for FM direction and/or rate, with response distributions suggesting that rate and directionality are independently represented in monkey primary auditory cortex. Little is known about the pattern of brain activity during processing of possible human language precursors, i.e., monkey vocalizations consisting of species-specific calls. During the passive listening stimulation in the acute 2-DG study described above, several different categories of sound stimuli were combined, among them monkey vocalizations. Several of these categories have now been investigated separately using [18F]2-fluoro-2-deoxyglucose and PET scanning across the same group of monkeys. The results demonstrate that the most rostral part of the STG, the temporal pole, where auditory activation columns were observed, is lateralized during the processing of species specific monkey vocalizations as demonstrated by significantly more activation of the left versus the right temporal pole. This is a reversal of the pattern observed for most of the STG where right hemisphere activation is generally greater than left. There was no significant hemispheric difference during low-level ambient sounds with activity in both hemispheres similar to the left-hemisphere during monkey vocalizations. This suggests the right hemisphere is suppressed during processing of monkey vocalizations and this was verified when monkeys with forebrain commissurotimies did not show the same temporal pole lateralization to monkey vocalizations. This lateralization of processing, demonstrated by left hemisphere dominance for species specific monkey calls, reveals a similar hemispheric processing pattern for monkey and human communication sounds and is dependent on the forebrain commissures.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Intramural Research (Z01)
Project #
1Z01MH001101-11
Application #
6675597
Study Section
National Institute of Mental Health Initial Review Group (NIMH)
Project Start
Project End
Budget Start
Budget End
Support Year
11
Fiscal Year
2002
Total Cost
Indirect Cost
Name
U.S. National Institute of Mental Health
Department
Type
DUNS #
City
State
Country
United States
Zip Code
Munoz, Monica; Mishkin, Mortimer; Saunders, Richard C (2009) Resection of the medial temporal lobe disconnects the rostral superior temporal gyrus from some of its projection targets in the frontal lobe and thalamus. Cereb Cortex 19:2114-30
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