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      Cortical Map Reorganization Enabled by Nucleus Basalis Activity

      1 , 1
      Science
      American Association for the Advancement of Science (AAAS)

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          Abstract

          Little is known about the mechanisms that allow the cortex to selectively improve the neural representations of behaviorally important stimuli while ignoring irrelevant stimuli. Diffuse neuromodulatory systems may facilitate cortical plasticity by acting as teachers to mark important stimuli. This study demonstrates that episodic electrical stimulation of the nucleus basalis, paired with an auditory stimulus, results in a massive progressive reorganization of the primary auditory cortex in the adult rat. Receptive field sizes can be narrowed, broadened, or left unaltered depending on specific parameters of the acoustic stimulus paired with nucleus basalis activation. This differential plasticity parallels the receptive field remodeling that results from different types of behavioral training. This result suggests that input characteristics may be able to drive appropriate alterations of receptive fields independently of explicit knowledge of the task. These findings also suggest that the basal forebrain plays an active instructional role in representational plasticity.

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          Most cited references34

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          Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys.

          Previous studies have shown that the tonotopic organization of primary auditory cortex is altered subsequent to restricted cochlear lesions (Robertson and Irvine, 1989) and that the topographic reorganization of the primary somatosensory cortex is correlated with changes in the perceptual acuity of the animal (Recanzone et al., 1992a-d). Here we report an increase in the cortical area of representation of a restricted frequency range in primary auditory cortex of adult owl monkeys that is correlated with the animal's performance at a frequency discrimination task. Monkeys trained for several weeks to discriminate small differences in the frequency of sequentially presented tonal stimuli revealed a progressive improvement in performance with training. At the end of the training period, the tonotopic organization of Al was defined by recording multiple-unit responses at 70-258 cortical locations. These responses were compared to those derived from three normal monkeys and from two monkeys that received the same auditory stimuli but that were engaged in a tactile discrimination task. The cortical representation, the sharpness of tuning, and the latency of the response were greater for the behaviorally relevant frequencies of trained monkeys when compared to the same frequencies of control monkeys. The cortical area of representation was the only studied parameter that was correlated with behavioral performance. These results demonstrate that attended natural stimulation can modify the tonotopic organization of Al in the adult primate, and that this alteration is correlated with changes in perceptual acuity.
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            Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6).

            Monoclonal antibodies to choline acetyltransferase and a histochemical method for the concurrent demonstration of acetylcholinesterase and horseradish peroxidase were used to investigate the organization of ascending cholinergic pathways in the central nervous system of the rat. The cortical mantle, the amygdaloid complex, the hippocampal formation, the olfactory bulb and the thalamic nuclei receive their cholinergic innervation principally, from cholinergic projection neurons of the basal forebrain and upper brainstem. On the basis of connectivity patterns, we subdivided these cholinergic neurons into six major sectors. The Ch1 and Ch2 sectors are contained within the medial septal nucleus and the vertical limb nucleus of the diagonal band, respectively. They provide the major cholinergic projections of the hippocampus. The Ch3 sector is contained mostly within the lateral portion of the horizontal limb nucleus of the diagonal band and provides the major cholinergic innervation to the olfactory bulb. The Ch4 sector includes cholinergic neurons in the nucleus basalis, and also within parts of the diagonal band nuclei. Neurons of the Ch4 sector provide the major cholinergic innervation of the cortical mantle and the amygdala. The Ch5-Ch6 sectors are contained mostly within the pedunculopontine nucleus of the pontomesencephalic reticular formation (Ch5) and within the laterodorsal tegmental gray of the periventricular area (Ch6). These sectors provide the major cholinergic innervation of the thalamus. The Ch5-Ch6 neurons also provide a minor component of the corticopetal cholinergic innervation. These central cholinergic pathways have been implicated in a variety of behaviors and especially in memory function. It appears that the age-related changes of memory function as well as some of the behavioral disturbances seen in the dementia of Alzheimer's Disease may be related to pathological alterations along central cholinergic pathways.
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              Acetylcholine and memory.

              Acetylcholine may set the dynamics of cortical networks to those appropriate for learning of new information, while decreased cholinergic modulation may set the appropriate dynamics for recall. In slice preparations of the olfactory cortex, acetylcholine selectively suppresses intrinsic but not afferent fiber synaptic transmission, while decreasing the adaptation of pyramidal cells. In biologically realistic models of this region, the selective suppression of synaptic transmission prevents recall of previously learned memories from interfering with the learning of new memories, while the decrease in adaptation enhances the response to afferent input and the modification of synapses. This theoretical framework may serve to guide future studies linking neuromodulators to cortical memory function.
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                Author and article information

                Journal
                Science
                Science
                American Association for the Advancement of Science (AAAS)
                0036-8075
                1095-9203
                March 13 1998
                March 13 1998
                : 279
                : 5357
                : 1714-1718
                Affiliations
                [1 ]Departments of Otolaryngology and Physiology, W. M. Keck Foundation Center for Integrative Neuroscience, University of California, San Francisco, 513 Parnassus Avenue, Box 0732, San Francisco, CA 94143, USA.
                Article
                10.1126/science.279.5357.1714
                9497289
                82c7ee6a-7e3d-488d-ac79-f510fb3d19e1
                © 1998
                History

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