Cognitive functions of the temporal lobe in the dog: A review

doi:10.1016/S0278-5846(00)00110-X

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volume 24, Issue 5, July 2000, Pages 855-880

https://doi.org/10.1016/S0278-5846(00)00110-X Get rights and content

Abstract

1.
1 The current paper reviews the role of temporal lobe structures in learning and different kinds of memory, with an emphasis on behavioral tasks that re auditory stimuli.
2.
2 The effects of lesions to structures in the temporal lobe were examined in separate groups of dogs, which were trained on an auditory spatial delayed response, or in a trial-unique auditory delayed match to sample recognition task.
3.
3 Spatial memory was impaired after bilateral hippocampal lesions. On the other hand, neither an anterior temporal lesion or rhinal cortical injury nor combined lesion to the hippocampus and the anterior temporal lobe, affected postoperative retraining and performance of the spatial task.
4.
4 Auditory recognition memory task was not impaired after a hippocampal and/or rhinal cortex lesion. However, postoperative retraining of the task was impaired after a lesion to auditory association areas.
5.
5 These results confirm the role of the hippocampus in spatial memory in the dog. On the other hand, the organization of auditory recognition functions within the temporal lobe appears to be different from those described for visual recognition functions.

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Lesions to the tonotopic auditory cortices, i.e., the middle and anterior ectosylvian areas, heavily impaired relearning on an auditory recognition task with trial-unique stimuli. Lesions to the non-tonotopic fields of the posterior ectosylvian, including additionally the composite posterior, and posterior sylvian areas also impaired performance on the recognition task, though the deficit was less pronounced [32,33]. Recent electrophysiological and connectivity results in the monkey indicate that processing of auditory information is arranged into dorsal and ventral intracortical streams, which can be separated already at the level of the thalamus [49–52,55].
The composite posterior and sylvian gyri of the canine temporal cortex show cytoarchitectonic features of poorly differentiated isocortex. Quantitative evaluation of connections examined with retrogradely transported fluorescent tracers indicated that both gyri received strong thalamic projections from the medial geniculate body (MG) and the lateromedial-suprageniculate (LM-Sg) complex, and a weaker projection from the posterior (Po) nuclei. On the basis of the connectivity patterns and cytoarchitectonic features we distinguished the anterior (CPa) and posterior (CPp) areas in posterior composite gyrus and the anterior (SA), dorsal (SD) and posterior (SP) sylvian areas. Afferents from individual thalamic nuclei were focused in distinct areas, forming dominant projections, and diminished gradually in the adjacent areas as non-dominant projections. The most prominent MG projection arose from the dorsal caudal (MGdc) nucleus. Its ventral subdivision sent a dominant projection into the SP and CPa, whereas the dorsal MGdc subdivision was connected with the SA, SD and CPp areas. The most substantial connections from the LM-Sg complex were directed to areas SA, SD and CPp, with weak connections to areas CPa and SP. A gradient of density of LM-Sg afferents was distributed in the opposite direction to that sent from the MGdc. The origin of the CPa and SP afferents in the ventral MGdc, like connections reaching the posterior ectosylvian cortex, suggest that these areas are related to processing of auditory information. In contrast, areas SA and CPp, receive dominant projections from the polymodal LM-Sg, and therefore may constitute successive steps in a hierarchy of cortical areas.
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- 1.
  1. The canine temporal cortex includes the ectosylvian, composite posterior and sylvian gyri.
- 2.
  2. The distinctive features of the canine temporal cortex include the ectosylvian sulcus closed in its dorsal side and the substantial development of neocortex located within the posterior composite gyrus.
- 3.
  3. Thalamofugal connections from particular nuclei of the medial geniculate body, posterior thalamus and lateromedial-suprageniculate complex project to specific areas of the canine temporal cortex and are arranged as dominant and non-dominant projections.
- 4.
  4. Local intracortical connections distinguish the ectosylvian and posterior composite areas as unimodal auditory cortex. Long distant connections and polymodal convergence indicate that the composite ectosylvian area of the anterior ectosylvian gyrus and the anterodorsal sylvian areas are higher order association cortex.
- 5.
  5. Analysis of both thalamo-cortical and intracortical connections indicate that auditory processing in the cortex occurs in successive, hierarchically organized stages and in two main, anterior and ventral pathways.
- 6.
  6. The functional significance and comparative aspects of connections are discussed.
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Cognitive functions of the temporal lobe in the dog: A review

Abstract

Neuropsychologia

Trends Neurosci.

Neuropsychologia

Brain Res.

Curr. Opin. Neurobiol.

Brain Res.

Neurosci. Lett.

Syndrome produced by lesions of the amygdala in monkeys (Macaca mulatta)

J. Comp. Physiol. Psychol.

Auditory frequency generalization with differing extinction influences in normal and prefrontal dogs trained in instrumental alimentary reflexes

Acta Neurobiol. Exp.

Four-pair same-different differentiation and transient memory in dogs

Acta Neurobiol. Exp.

Impairment of auditory recent memory produced by cortical lesions in dogs

Acta Biol. Exp.

Non-verbal auditory recognition in normal subjects and brain-damaged patients: Evidence for parallel processing

Neuropsychologia

A comparison of visual and auditory short-term memory in monkeys (Cebus apella)

Quart.J. Exp. Psychol.

Dissociation of impairment after lateral and medial prefrontal lesions in dogs

Science

Prefrontal lesions and avoidance reflex differentiation in dogs

Acta Neurobiol. Exp.

Auditory matching-to-sample in monkeys (Cebus apella)

Animal Learning Behav.

Discrimination of auditory sequences by monkeys

Nature

Auditory discrimination and recall in monkeys

Science

Selective hippocampal lesions yield nonspatial memory impairment in rhesus monkeys. Rapid communication

Hippocampus

The role of the hypothalamus and amygdala in food intake alimentary motivation and emotional reactions

Acta Biol. Exp.

Control of emotional behavior through the hypothalamus and amygdaloid complex

The suppressing effect of chloropromazine treatment on alimentary-social differentiation in amygdala dogs

Integr. Physiol. Behav. Sci.

Cortical connections of the somatosensory fields of the lateral sulcus of macaques: evidence for a cortico-limbic pathway for touch

J. Comp. Neurol.

Auditory recognition memory in the rhesus monkey: behavioral training procedure

Soc. Neurosci. Abstr.

Recognition impaired and association intact in the memory of monkeys after transection of the fornix

J. Comp. Physiol. Psychol.

Amygdalar interaction with the mediodorsal nucleus of the thalamus and the ventromedial prefrontal cortex in stimulus-reward associative learning in the monkey

J. Neurosci.

Interaction of the amygdala with the frontal lobe in reward memory

European J. Neurosci.

Effect of auditory cortex ablation on localization and discrimination of brief sounds

J. Neurophysiol.

An anatomical study of converging sensory pathways within the cerebral cortex of the monkey

Brain

Auditory short-term memory in the Japanese monkey

Internat.J. Neurosci.

Subcortical connections of the prefrontal cortex in dog's brain: afferents to the proreal gyrus

Acta Neurobiol. Exp.

Topographical organization of the frontal association cortex afferents originating in the ventral thalamic nuclei in dog brain

Acta Neurobiol. Exp.

Organization of connections underlying the processing of auditory information in the dog

Subcortical connections of the prefrontal cortex in dog's brain: Afferents to the orbital gyrus

Acta Neurobiol. Exp.

Thalamic and amygdaloid connections of the auditory association cortex of the superior temporal gyrus in rhesus monkey (Macaca mulatta)

Acta Neurobiol. Exp.

The presylvian cortex as a transitional prefronto-motor zone in dog

Acta Neurobiol. Exp.

Amphetamine increases intertrial but not conditional instrumental responding in the cortico-basomedial amygdalar dogs

Pavlov J. Biol. Sci.

Extinction of generalized avoidance responses during the acquisition of go, no-go differentiation with symmetrical and asymmetrical reinforcement (in Russian)

Effects of hippocampal lesions on spatial delayed responses in dogs

Hippocampus

The methods of training dogs in auditory recognition memory tasks with trial-unique stimuli

Acta Neurobiol. Exp.

Effects of the anterior temporal lobe lesions, separate or combined with the hippocampus, on spatial delayed responses guided by auditory stimulus

Acta Neurobiol. Exp.

Effects of partial prefrontal lesions in dogs on go — no go avoidance reflex differentiation and reversal learning

Acta Neurobiol. Exp.

Retention of symmetrical go no go avoidance differentiation after prefrontal lesions in dogs

Bull. Acad. Pol. Sci. Ser. Sci. Biol.

The method of surgical hippocampal lesions in dogs

Acta Neurobiol. Exp.