Context-dependent responses of primate nucleus basalis neurons in a go/no-go task

In previous studies involving monkeys performing behavioral tasks, neurons in the nucleus basalis frequently had significant changes in discharge rate when the animal made a movement in response to a sensory stimulus in order to obtain a reward. To determine whether such responses of basalis neurons are primarily sensory or motor in nature, the activity of single basalis neurons was recorded in monkeys performing a go/no-go (GNG) task which provided a dissociation between sensory and motor neuronal responses. In a sample of 425 basalis neurons, 326 (77%) had significant changes in firing in at least one phase of the GNG task. Most of the task-related neurons (70%) responded in the choice phase in which the animal either made an arm movement (go condition) or kept its arm motionless (no-go condition) in order to obtain a water reward. Of 253 neurons that responded in the choice phase, 88% had changes in firing in the no-go condition that were equal to or, in some cases, greater than the changes in firing in the go condition. Therefore, most responses of basalis neurons in the choice phase could not be specific for the arm movement because they occurred when there was no arm movement at all. The visual stimulus presented in the choice phase was also presented earlier on each trial in the cue phase. Although 70% of the task-related basalis neurons responded in the choice phase, only 5% had detectable changes in firing in the cue phase. Of 251 neurons responding in the cue or choice phase, 59% had significantly larger changes in firing in the choice phase than in the cue phase, whereas only one neuron had a larger response in the cue phase. Therefore, most responses of basalis neurons in the choice phase could not be specific for the visual stimulus because similar responses did not occur when the same stimulus was presented in the cue phase. These results indicate that the frequent responses of basalis neurons in the choice phase are neither purely sensory nor motor in nature, but are highly dependent on the context of the stimulus or movement. The neuronal responses in the choice phase may reflect either transient increases in arousal or decision-making processes.

[1]  C. Shute,et al.  The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. , 1967, Brain : a journal of neurology.

[2]  M. Delong,et al.  Activity of pallidal neurons during movement. , 1971, Journal of neurophysiology.

[3]  J. Fuster Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[4]  G. Pepeu The release of acetylcholine from the brain: an approach to the study of the central cholinergic mechanisms. , 1973, Progress in neurobiology.

[5]  Chapter 2 – Cholinergic Roles in Consciousness , 1974 .

[6]  Masataka Watanabe,et al.  Prefrontal unit activity and delayed response: Relation to cue location versus direction of response , 1976, Brain Research.

[7]  D. Rasmusson,et al.  Acetylcholine release from visual and sensorimotor cortices of conditioned rabbits: The effects of sensory cuing and patterns of responding , 1976, Brain Research.

[8]  E. T. Rolls,et al.  Hypothalamic neuronal responses associated with the sight of food , 1976, Brain Research.

[9]  E. Rolls,et al.  Modulation during learning of the responses of neurons in the lateral hypothalamus to the sight of food , 1976, Experimental Neurology.

[10]  E. Rolls,et al.  Effects of hunger on the responses of neurons in the lateral hypothalamus to the sight and taste of food , 1976, Experimental Neurology.

[11]  E. Rolls,et al.  The latency of activation of neurones in the lateral hypothalamus and substantia innominata during feeding in the monkey , 1979, Brain Research.

[12]  A. Levey,et al.  Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey , 1983, The Journal of comparative neurology.

[13]  C. H. Vanderwolf,et al.  Cholinergic activation of the electrocorticogram: Role of the substantia innominata and effects of atropine and quinuclidinyl benzilate , 1984, Brain Research.

[14]  D. Collerton,et al.  Cholinergic function and intellectual decline in Alzheimer's disease , 1986, Neuroscience.

[15]  J. Coyle,et al.  Basal forebrain neurons provide major cholinergic innervation of primate neocortex , 1986, Neuroscience Letters.

[16]  G. Rigdon,et al.  Nucleus basalis involvement in conditioned neuronal responses in the rat frontal cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  R. Szymusiak,et al.  Sleep-related neuronal discharge in the basal forebrain of cats , 1986, Brain Research.

[18]  M. Delong,et al.  Nucleus basalis of Meynert neuronal activity during a delayed response task in monkey , 1986, Brain Research.

[19]  Differential responses of nucleus basalis of meynert neurons in a go no go task in monkey macaca mulatta , 1986 .

[20]  M. Mesulam,et al.  Three-dimensional representation and cortical projection topography of the nucleus basalis (Ch4) in the macaque: concurrent demonstration of choline acetyltransferase and retrograde transport with a stabilized tetramethylbenzidine method for horseradish peroxidase , 1986, Brain Research.

[21]  A. Levey,et al.  Cholinergic nucleus basalis neurons may influence the cortex via the thalamus , 1987, Neuroscience Letters.

[22]  C. H. Vanderwolf,et al.  Activity of identified cortically projecting and other basal forebrain neurones during large slow waves and cortical activation in anaesthetized rats , 1987, Brain Research.

[23]  A. Parent,et al.  Cholinergic and non-cholinergic neurons of cat basal forebrain project to reticular and mediodorsal thalamic nuclei , 1987, Brain Research.

[24]  A test for a threshold in an ordered sequence of correlated proportions. , 1987, Biometrics.

[25]  M. Delong,et al.  A reappraisal of the functions of the nucleus basalis of Meynert , 1988, Trends in Neurosciences.

[26]  G. Buzsáki,et al.  Nucleus basalis and thalamic control of neocortical activity in the freely moving rat , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[27]  R. Vertes Brainstem afferents to the basal forebrain in the rat , 1988, Neuroscience.

[28]  M. Delong,et al.  Responses of Nucleus Basalis of Meynert Neurons in Behaving Monkeys , 1988 .

[29]  H. Fibiger,et al.  Brainstem afferents to the magnocellular basal forebrain studied by axonal transport, immunohistochemistry, and electrophysiology in the rat , 1988, The Journal of comparative neurology.

[30]  J. Krystal,et al.  Psychopharmacology: The Third Generation of Progress , 1989, The Yale Journal of Biology and Medicine.