Evidence for a cholinergic projection to neocortex from neurons in basal forebrain.

Johnston, Michael V.; McKinney, Michael; Coyle, Joseph T.

doi:10.1073/pnas.76.10.5392

Cited by 326 publications

(118 citation statements)

References 49 publications

Supporting

Mentioning

112

Contrasting

Unclassified

Order By: Relevance

“…The NB is the main source of cortical ACh 93,94 and there is extensive evidence for the importance of ACh and of the NB in particular in many aspects of learning (reviewed in REF. 33).…”

Section: The Nb Cholinergic Systemmentioning

confidence: 99%

Specific long-term memory traces in primary auditory cortex

2004

View full text Add to dashboard Cite

Learning and memory involve the storage of specific sensory experiences. However, until recently the idea that the primary sensory cortices could store specific memory traces had received little attention. Converging evidence obtained using techniques from sensory physiology and the neurobiology of learning and memory supports the idea that the primary auditory cortex acquires and retains specific memory traces about the behavioural significance of selected sounds. The cholinergic system of the nucleus basalis, when properly engaged, is sufficient to induce both specific memory traces and specific behavioural memory. A contemporary view of the primary auditory cortex should incorporate its mnemonic and other cognitive functions.Identifying the neural substrates of learning and memory is a core problem in neuroscience. As memories involve the representation of past sensory events, they may be stored, in part, within sensory systems. Sensory systems have traditionally been viewed as 'stimulus analysers', with learning and memory assigned to 'higher' cortical regions. Nonetheless, neurophysiological studies have produced evidence for learning-induced plasticity in sensory cortices, and in particular the auditory cortex. Galambos and colleagues first implicated the primary auditory cortex (A1) in learning in 1956, observing that pairing an auditory conditioned stimulus (CS) with a weak shock (a mildly aversive unconditioned stimulus (US)) produced a significant increase in the amplitude of CS-elicited evoked field potentials in A1 of the cat 1 . Subsequently, these findings were extended to other tasks (such as discrimination), types of learning (including instrumental conditioning), motivations (for example, food) and types of recording (such as single and multiple unit discharges) 2 .Although such results established associative plasticity in A1, neither they nor similar findings in other sensory cortices addressed the key issue of specificity of information storage. As memories have specific content, how could changes in the magnitude of sensory cortical responses adequately reflect the encoding of specific aspects of experiences? A solution was provided by the field of sensory neurophysiology, which focuses on stimulus specificity. Sensory physiology experiments use a wide range of stimulus values to NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript determine how specific sensory stimuli are processed and coded. In fact, the basic paradigms of sensory physiology and learning are complementary (Box 1).This article presents an overview of research that combines experimental designs from sensory physiology with those of learning and memory to search for specific memory traces in A1. A sign of a specific memory trace would be learning-induced physiological plasticity that has the key characteristics of behavioural memory and sufficient specificity to encode a canonical attribute of experience, such as a physical feature and its behavioural importance. Previous reviews have covered ot...

show abstract

“…The NB is the main source of cortical ACh 93,94 and there is extensive evidence for the importance of ACh and of the NB in particular in many aspects of learning (reviewed in REF. 33).…”

Section: The Nb Cholinergic Systemmentioning

confidence: 99%

Specific long-term memory traces in primary auditory cortex

2004

View full text Add to dashboard Cite

show abstract

“…All of the stimulation sites were located within the basal forebrain in structures containing corticopetal cholinergic cells, including those that project to the ipsilateral auditory cortex (Bigl et al, 1982;Johnston et al, 1979;Luiten et al, 1987;Mesulam et al, 1983;Rye et al, 1984) (Figure 2C). …”

Section: Effectiveness Of Nb Stimulationmentioning

confidence: 99%

“…The nucleus basalis of the basal forebrain (NB) is the major source of extrinsic acetylcholine (ACh) to the cerebral cortex (Bigl, Woolf, & Butcher, 1982;Johnston, McKinney, & Coyle, 1979;Luiten, Gaykema, Traber, & Spencer, 1987;Mesulam, Mufson, Wainer, & Levey, 1983;Rye, Wainer, Mesulam, Mufson, & Saper, 1984). Activation of the NB to release ACh in the cerebral cortex has a profound effect on cortical state.…”

Section: Introductionmentioning

confidence: 99%

Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory

Miasnikov

Chen

Gross

et al. 2008

Neurobiology of Learning and Memory

View full text Add to dashboard Cite

The cholinergic system has been implicated in learning and memory. The nucleus basalis (NB) provides acetylcholine (ACh) to the cerebral cortex. Pairing a tone with NB stimulation (NBstm) to alter cortical state induces both associative specific tuning plasticity in the primary auditory cortex (A1) and associative specific auditory behavioral memory. NB-induced memory has major features of natural memory that is induced by pairing a tone with motivational reinforcers, e.g., food or shock, suggesting that the cholinergic system may be a "final common pathway" whose activation promotes memory storage. Alternatively, NB-stimulation might itself be motivationally significant, either rewarding or punishing. To investigate these alternatives, adult male rats (n = 7) first formed a specific NB-induced memory (CS = 8.0 kHz, 2.0 s paired with NBstm, ISI = 1.8 s, 200 trials), validated by post-training (24 h) frequency generalization gradients (1-15 kHz) of respiration interruption that were specific to the CS frequency. Thereafter, they received the same level of NBstm that had induced memory, while confined to one quadrant of an arena, and later tested for place preference, i.e., avoidance or seeking of the quadrant of NBstm. This NBstm group exhibited neither preference for nor against the stimulated quadrant, compared to sham-operated subjects (n = 7). The findings indicate that specific associative memory can be induced by direct activation of the NB without detectable motivational effects of NB stimulation. These results are concordant with a memorypromoting role for the nucleus basalis that places it "downstream" of motivational systems, which activate it to initiate the storage of the current state of its cholinergic targets.

show abstract

“…All rats quickly returned to the criterion level of performance when the delay was decreased to 5 sec. nergic, serotonergic, and histaminergic afferents (Johnston et al, 1979(Johnston et al, , 1981 (Davis and Yamamura, 1978;Perry et al, 1978;.…”

Section: Blocks Of Two Test Sessionsmentioning

confidence: 99%

Lesions in nucleus basalis magnocellularis and medial septal area of rats produce qualitatively similar memory impairments

Hepler¹,

Olton²,

Wenk³

et al. 1985

J. Neurosci.

382

View full text Add to dashboard Cite

The functional contribution of nucleus basalis magnocellularis (NBM) and the medial septal area (MSA) to memory was evaluated in two different spatial discriminations. Preoperatively, rats were trained to a criterion level of performance in a simultaneous left/right discrimination on the stem of a T-maze (a trial-independent memory) and a discretetrial, rewarded alternation discrimination on the arms of the T-maze (a trial-dependent memory). Bilateral lesions were made by injecting ibotenic acid (IBO) into the NBM, MSA, both NBM and MSA, or dorsal globus pallidus (DGP), and by radiofrequency current (RF) in the NBM and MSA. Control rats received operations in which either no current was passed or no neurotoxin was injected. Lesions in the NBM, MSA, or both the NBM and MSA produced a similar pattern of behavioral changes relative to the performance of controls; postoperative reacquisition of the arm discrimination was initially impaired but showed recovery to normal levels, whereas postoperative reacquisition and reversal of the stem discrimination was not impaired (except following the combined NBM and MSA lesion). Lesions of the DGP had no effect on choice accuracy in any discrimination.When the discrimination on the arms was made more difficult by increasing the delay interval during which the information had to be remembered, rats with combined NBM and MSA lesions were again impaired relative to controls and showed no signs of recovery of function. These results provide information about the behavioral functions of the basal forebrain cholinergic system and suggest that pathological changes in certain components of this system can cause disorders of memoryWithin the basal forebrain of the rat is a core of acetylcholinergic (ACh) neurons (Sofroniew et al., 1982) (NBM), diagonal band of Broca, and the medial septal area (MSA) Lehmann et al., 1980;Johnston et al., 1981;Bigl et al., 1982;Hartgraves et al., 1982; Pearson et al., 1983; Saper, 1984). The NBM projects ACh afferents primarily to the neocortex, and the MSA and vertical limb of the diagonal band project ACh afferents primarily to the hippocampus. The frontal neocortex and hippocampus, and the cholinergic systems afferent to these areas, have an important role in memory (Bartus, 1980; Bartus et al., 1982; Mishkin, 1982). Recently, the behavioral effects of lesions produced in either the NBM (LoConte et al., 1982; Flicker et al., 1983) or MSA (Mitchell et al., 1982) have been evaluated separately in individual tasks, but the behavioral effects of these two lesions have not been compared on the same tasks.In the present study, both ibotenic acid (IBO) and radiofrequency (RF) current were used to produce lesions. IBO causes degeneration of neuronal perikarya at the site of injection, without damaging axons of passage or neurons distant from the injection site (Coyle and Schwartz, 1983). RF lesions destroy both neuronal perikarya and fibers of passage. The comparison of RF and IBO lesions allows for the assessment of the relative importance of d...

show abstract

Evidence for a cholinergic projection to neocortex from neurons in basal forebrain.

Cited by 326 publications

References 49 publications

Specific long-term memory traces in primary auditory cortex

Specific long-term memory traces in primary auditory cortex

Motivationally neutral stimulation of the nucleus basalis induces specific behavioral memory

Lesions in nucleus basalis magnocellularis and medial septal area of rats produce qualitatively similar memory impairments

Contact Info

Product

Resources

About