Selective memory loss following nucleus basalis lesions: Long term behavioral recovery despite persistent cholinergic deficiencies

Bartus, Raymond T.; Flicker, Charles; Dean, Reginald L.; Pontecorvo, Michael J.; Figueiredo, Joanne C.; Fisher, Stephen K.

doi:10.1016/0091-3057(85)90139-x

Cited by 249 publications

(69 citation statements)

References 62 publications

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“…The cortical BF shift becomes long-lasting, but the lengthening the recovery time of the collicular BF shift is small (63). (77)(78)(79). (iv) The basal forebrain receives an input from the amygdala, which is necessary for the acquisition of conditioned response (80)(81)(82).…”

Section: Corticofugal Modulation and Plasticity Of The Auditory Systementioning

confidence: 99%

The corticofugal system for hearing: Recent progress

Suga

Gao

Zhang

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

228

170

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Peripheral auditory neurons are tuned to single frequencies of sound. In the central auditory system, excitatory (or facilitatory) and inhibitory neural interactions take place at multiple levels and produce neurons with sharp level-tolerant frequency-tuning curves, neurons tuned to parameters other than frequency, cochleotopic (frequency) maps, which are different from the peripheral cochleotopic map, and computational maps. The mechanisms to create the response properties of these neurons have been considered to be solely caused by divergent and convergent projections of neurons in the ascending auditory system. The recent research on the corticofugal (descending) auditory system, however, indicates that the corticofugal system adjusts and improves auditory signal processing by modulating neural responses and maps. The corticofugal function consists of at least the following subfunctions. auditory system ͉ descending system ͉ learning and memory ͉ plasticity ͉ tonotopic map T he central auditory system creates many physiologically distinct types of neurons for auditory signal processing. Their response properties have been interpreted to be produced by divergent and convergent interactions between neurons in the ascending auditory system. Until recently, the contribution of the descending (corticofugal) system to the shaping (or even creation) of their response properties has hardly been considered. Recent findings indicate that the corticofugal system plays important roles in shaping or even creating the response properties of central auditory neurons and in reorganizing cochleotopic (frequency) and computational (e.g., echo-delay) maps. Therefore, the understanding of the neural mechanisms for auditory signal processing is incomplete without the exploration of the functional roles of the corticofugal system. In this article, we first enumerate several types of neurons and computational maps created in the bat's central auditory system and then describe the anatomy and physiology of the corticofugal system. Neurons Tuned to Acoustic Parameters Characterizing Biosonar Signals and Cochleotopic and Computational MapsAll peripheral neurons are tuned to single frequencies (best frequencies, BFs). In the central auditory system, excitatory, inhibitory, and facilitatory neural interactions take place at multiple levels and produce neurons with sharp level-tolerant (the width of a frequency tuning curve is narrow regardless of sound levels) frequency tuning curves (1) and also neurons tuned to specific values of parameters other than frequency. Some of these neurons apparently are related to the processing of biosonar signals. They are latency-constant, phasic on-responding neurons (2, 3); paradoxical latency-shift neurons (4); durationtuned neurons (5) amplitude coordinates for the fine spatio-temporal representation of periodic frequency and amplitude modulations of echoes from flying insects (9). In the superior colliculus of the big brown bat, there is a space map, and some neurons are tuned to a sound source at ...

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Section: Corticofugal Modulation and Plasticity Of The Auditory Systementioning

confidence: 99%

The corticofugal system for hearing: Recent progress

Suga

Gao

Zhang

et al. 2000

Proc. Natl. Acad. Sci. U.S.A.

228

170

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“…It is thus very unlikely that muscimol applied to the somatosensory cortex inactivated the AC. (18)(19)(20). (iv) The basal forebrain receives an input from the amygdala, which is necessary for the acquisition of conditioned response (21)(22)(23).…”

Section: Effects Of Bilateral Inactivation Of the Somatosensory Cortementioning

confidence: 99%

Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: Role of the corticofugal system

Gao

Suga

2000

Proc. Natl. Acad. Sci. U.S.A.

224

154

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In the big brown bat, Eptesicus fuscus, the response properties of neurons and the cochleotopic (frequency) maps in the auditory cortex (AC) and inferior colliculus can be changed by auditory conditioning, weak focal electric stimulation of the AC, or repetitive delivery of weak, short tone bursts. The corticofugal system plays an important role in information processing and plasticity in the auditory system. Our present findings are as follows. In the AC, best frequency (BF) shifts, i.e., reorganization of a frequency map, slowly develop and reach a plateau Ϸ180 min after conditioning with tone bursts and electric-leg stimulation. The plateau lasts more than 26 h. In the inferior colliculus, on the other hand, BF shifts rapidly develop and become the largest at the end of a 30-min-long conditioning session. The shifted BFs return (i.e., recover) to normal in Ϸ180 min. The collicular BF shifts are not a consequence of the cortical BF shifts. Instead, they lead the cortical BF shifts. The collicular BF shifts evoked by conditioning are very similar to the collicular and cortical BF shifts evoked by cortical electrical stimulation. Therefore, our working hypothesis is that, during conditioning, the corticofugal system evokes subcortical BF shifts, which in turn boost cortical BF shifts. The cortical BF shifts otherwise would be very small. However, whether the cortical BF shifts are consequently boosted depends on nonauditory systems, including nonauditory sensory cortices, amygdala, basal forebrain, etc., which determine the behavioral relevance of acoustic stimuli.associative learning ͉ conditioning ͉ hearing ͉ reorganization of tonotopic map ͉ somatosensory cortex T he response properties of neurons and the sensory map in a sensory cortex and subcortical sensory nucleus can be changed by conditioning, learning of a discrimination task, or focal cortical electrical stimulation (see refs. 1-3 for reviews). In the central nucleus of the inferior colliculus (IC) of the big brown bat, Eptesicus fuscus, the best frequency (BF) of a neuron shifts toward the frequency of a conditioned tone that is followed by an unconditioned electric leg stimulus (ES l ). The BF shift of Ϸ1.5 kHz lasts up to 180 min after a 30-min-long conditioning session. Inactivation of the primary auditory cortex (AC) during the conditioning abolishes the collicular BF shift that otherwise would be evoked (4). Focal electrical stimulation of the AC evokes collicular (5, 6) and cortical BF shifts (6, 7) very similar in the amount and duration (retention) to the collicular BF shift evoked by the conditioning. These data indicate that the collicular BF shift evoked by the conditioning is produced by the corticofugal system but do not indicate whether the collicular BF shift is due to the cortical BF shift or vice versa. It has not yet been determined which is the case, because it is very difficult, if not impossible, to inactivate corticofugal fibers selectively without inactivating thalamocortical fibers. One of the aims of the present paper is to p...

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“…Early studies suggested an important role for this system in learning and memory. Rats with ibotenic acid lesions of the nucleus basalis magnocellularis/substantia innominata (nBM/SI), the component of the basal forebrain that projects predominantly to neocortex, were impaired on a preoperatively learned delayed nonmatching-tosample (DNMS) radial maze task (Bartus et al 1985b(Bartus et al , 1986. Similarly, lesions to the nBM/SI or medial septum/vertical limb of the diagonal band (MS/VDB; the component of the basal forebrain that projects predominantly to the hippocampus) also impaired learning and performance in spatial working memory in the radial arm maze (Hepler et al 1985;M'Harzi and Jarrard 1992).…”

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confidence: 99%

Extensive Lesions of Cholinergic Basal Forebrain Neurons Do Not Impair Spatial Working Memory

Vuckovich

Semel²,

Baxter³

2004

Learn. Mem.

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A recent study suggests that lesions to all major areas of the cholinergic basal forebrain in the rat (medial septum, horizontal limb of the diagonal band of Broca, and nucleus basalis magnocellularis) impair a spatial working memory task. However, this experiment used a surgical technique that may have damaged cerebellar Purkinje cells. The present study tested rats with highly selective lesions of cholinergic neurons in all major areas of the basal forebrain on a spatial working memory task in the radial arm maze. In postoperative testing, there were no significant differences between lesion and control groups in working memory, even with a delay period of 8 h, with the exception of a transient impairment during the first 2 d of postoperative testing at shorter delays (0 or 2 h). This finding corroborates other results that indicate that the cholinergic basal forebrain does not play a significant role in spatial working memory. Furthermore, it underscores the presence of intact memory functions after cholinergic basal forebrain damage, despite attentional impairments that follow these lesions, demonstrated in other task paradigms.The cognitive functions of the basal forebrain cholinergic system (BFCS) are of considerable interest, given the damage to this system associated with neuropathological conditions such as Alzheimer's disease (Perry et al. 1977(Perry et al. , 1978Bartus et al. 1982Bartus et al. , 1985aBaxter and Gallagher 1997;Bartus 2000). Experimental lesion studies have attempted to address the question of which aspects of cognitive impairment in these human disease states, if any, can be attributed to loss of cholinergic neurons. The present study aims to further clarify the role of the BFCS in spatial cognition.The extent of acetylcholine loss in aged and demented subjects correlates with the extent of their cognitive impairment (Perry et al. 1977(Perry et al. , 1978Bartus et al. 1982). Experiments on animals have therefore examined the effects of BFCS lesions on spatial learning and memory tasks. These tasks are thought to effectively model the cognitive processes that are usually the first to deteriorate in aged and demented humans (Gallagher and Pelleymounter 1988). However, different BFCS lesion experiments have produced seemingly contradictory results. Early studies suggested an important role for this system in learning and memory. Rats with ibotenic acid lesions of the nucleus basalis magnocellularis/substantia innominata (nBM/SI), the component of the basal forebrain that projects predominantly to neocortex, were impaired on a preoperatively learned delayed nonmatching-tosample (DNMS) radial maze task (Bartus et al. 1985b(Bartus et al. , 1986. Similarly, lesions to the nBM/SI or medial septum/vertical limb of the diagonal band (MS/VDB; the component of the basal forebrain that projects predominantly to the hippocampus) also impaired learning and performance in spatial working memory in the radial arm maze (Hepler et al. 1985;M'Harzi and Jarrard 1992).However, studies using ibotenic acid ca...

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Selective memory loss following nucleus basalis lesions: Long term behavioral recovery despite persistent cholinergic deficiencies

Cited by 249 publications

References 62 publications

The corticofugal system for hearing: Recent progress

The corticofugal system for hearing: Recent progress

Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: Role of the corticofugal system

Extensive Lesions of Cholinergic Basal Forebrain Neurons Do Not Impair Spatial Working Memory

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