Afferent discharges to the cerebral cortex from peripheral sense organs

Adrian, E. D.

doi:10.1113/jphysiol.1941.sp003932

Cited by 401 publications

(77 citation statements)

References 7 publications

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“…Excitatory and inhibitory neurons in the cortex are never electrically silent, even in the absence of specific sensory (or cognitive) stimuli. High resting neuronal activity has been acknowledged since the earliest microscopic or macroscopic electrical recordings made from anesthetized or awake animals (56,57). Nonetheless it took years of research, recently guided by 13 C MRS and calibrated fMRI, to establish the high energetic cost of activity at rest and then to show that differencing it away discards a large fraction of the total energy needed for function.…”

Section: Discussionmentioning

confidence: 99%

Energetics of neuronal signaling and fMRI activity

Maandag

Coman

Sanganahalli

et al. 2007

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

124

125

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Energetics of resting and evoked fMRI signals were related to localized ensemble firing rates () measured by electrophysiology in rats. Two different unstimulated, or baseline, states were established by anesthesia. Halothane and ␣-chloralose established baseline states of high and low energy, respectively, in which forepaw stimulation excited the contralateral primary somatosensory cortex (S1). With ␣-chloralose, forepaw stimulation induced strong and reproducible fMRI activations in the contralateral S1, where the ensemble firing was dominated by slow signaling neurons (SSN; range of 1-13 Hz). Under halothane, weaker and less reproducible fMRI activations were observed in the contralateral S1 and elsewhere in the cortex, but ensemble activity in S1 was dominated by rapid signaling neurons (RSN; range of 13-40 Hz). For both baseline states, the RSN activity (i.e., higher frequencies, including the ␥ band) did not vary upon stimulation, whereas the SSN activity (i.e., ␣ band and lower frequencies) did change. In the high energy baseline state, a large majority of total oxidative energy [cerebral metabolic rate of oxygen consumption (CMR O2)] was devoted to RSN activity, whereas in the low energy baseline state, it was roughly divided between SSN and RSN activities. We hypothesize that in the high energy baseline state, the evoked changes in fMRI activation in areas beyond S1 are supported by rich intracortical interactions represented by RSN. We discuss implications for interpreting fMRI data where stimulus-specific ⌬CMR O2 is generally small compared with baseline CMR O2.awake ͉ behavior ͉ calibrated fMRI ͉ glucose ͉ glutamate N oninvasive NMR and electrophysiological methods offer considerably different spatiotemporal results that presumably reflect the same cerebral activity. Localized energy consumption of neuronal and glial populations in MRI voxels has been evaluated (1), initially from 13 C MRS (2) and more recently from calibration of functional MRI (fMRI) (3). In vivo electrophysiological measurements of neuronal activity, from single neurons or large ensembles (4), are considered the gold standard of cerebral activity (5). Can measurements from these dissimilar techniques provide complementary insights into the working brain?A promising convergence between these apparently different results relies on a universal thermodynamic principle, the fundamental relationship between the work done and the energy expended. Cerebral energy comes almost exclusively from glucose oxidation (6). Recent results have shown that the cerebral metabolic rate of oxygen consumption (CMR O2 ) is almost completely dedicated to supporting work associated with synaptic activity (7,8). Changes in CMR O2 from calibrated fMRI (9) are linear with changes in firing rates of a representative neuronal ensemble in the same voxel (10). This basic work/ energy relationship has been extended by in vivo investigations (11, 12) that relate imaging energetics to the underlying neuronal activities.Neuroimaging methods localize changes of task-i...

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Section: Discussionmentioning

confidence: 99%

Energetics of neuronal signaling and fMRI activity

Maandag

Coman

Sanganahalli

et al. 2007

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

124

125

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“….no removal of cortex anywhere can prevent pain from being felt and only very rarely does a patient use the word pain to describe the result of cortical stimulation ", and, he goes on, " it is obvious therefore that the pathway of pain conduction reaches the thalamus and consciousness without essential conduction to the cortex ". Adrian (1941) found that no impulses reached the sensory cortex in response to noxious or thermal stimulation at the periphery in the rabbit, cat, and monkey. On the other hand, a considerable body of evidence would suggest that there is central representation of pain in the cortex, and this work has been summarized recently by Marshall (1951) who, in presenting further evidence from 11 cases of cortical wounds followed by impairment of pain and temperature sense, advanced the hypothesis that the final elaboration of sensory impulses depends on mutual activation of thalamus and cortex.…”

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confidence: 96%

Observations on Partial Removal of the Post-Central Gyrus for Pain

Lewin¹,

Phillips²

1952

Journal of Neurology, Neurosurgery & Psychiatry

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The role of the cerebral cortex in the conscious appreciation of pain has interested neurologists for many years. Head and Holmes (1911) considered that pain entered consciousness at thalamic level, and more recently Penfleld (1947) stated that 6. . .no removal of cortex anywhere can prevent pain from being felt and only very rarely does a patient use the word pain to describe the result of cortical stimulation ", and, he goes on, " it is obvious therefore that the pathway of pain conduction reaches the thalamus and consciousness without essential conduction to the cortex ". Adrian (1941) found that no impulses reached the sensory cortex in response to noxious or thermal stimulation at the periphery in the rabbit, cat, and monkey. On the other hand, a considerable body of evidence would suggest that there is central representation of pain in the cortex, and this work has been summarized recently by Marshall (1951) who, in presenting further evidence from 11 cases of cortical wounds followed by impairment of pain and temperature sense, advanced the hypothesis that the final elaboration of sensory impulses depends on mutual activation of thalamus and cortex.Electrical stimulation of the cortex has yielded equivocal results. In Cushing's (1909) two cases stimulation of the post-central gyrus was painless, and Foerster (1936) reported paraesthesiae but seldom pain. Penfield and Boldrey (1937) recorded only 11 instances out of well over 800 responses to electrical stimulation where the word " pain" had been used by the patient to describe the cortical sensation. Recently, however, Horrax (1946) stimulated the post-central gyrus in four patients suffering from painful states and elicited pain in three. To explain the apparent discrepancy between his results and those of Penfield and Boldrey, Horrax concluded that he was probably using too strong a current, since in the motor cortex the same current caused convulsions. Stone (1950) also recorded one case where stimulation of the sensory cortex produced pain in the phantom leg.In this paper we wish to record three cases in which partial resection of the post-central gyrus was undertaken for the relief of pain. In the first patient the pain developed during an unusual, prolonged, sensory painful aura in traumatic epilepsy, the second patient had intractable pain in a phantom foot, and the third had a painful thigh stump. In all three, electrical stimulation of the appropriate area of the post-central gyrus reproduced the pain complained of by the patient and relief followed the removal of this area of cortex. Results of StimulationThe operations were conducted under local analgesia. Monopolar stimulation was used. The stimulator gave negative square pulses of current, the strength, frequency, and duration of which could be independently controlled. The position of the motor cortex was first identified by stimulation and then the post-central gyrus was explored. With varying parameters, different thresholds of stimulation in the motor and sensory cortex were established. ...

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“…An afferent volley from a peripheral nerve evokes a diphasic potential on the surface of the somatosensory cortex which has an initial positivity and a late negativity (12)(13)(14). Al though it is only imprecisely understood (15), it is generally believed that the initial effect is Each point represents an average of 32 consecutive evoked potentials.…”

Section: Discussionmentioning

confidence: 99%

Effect of Carbachol on the Somatosensory Evoked Potentials in the Rat

Bhargava

1971

Jpn.J.Pharmacol

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Afferent discharges to the cerebral cortex from peripheral sense organs

Cited by 401 publications

References 7 publications

Energetics of neuronal signaling and fMRI activity

Energetics of neuronal signaling and fMRI activity

Observations on Partial Removal of the Post-Central Gyrus for Pain

Effect of Carbachol on the Somatosensory Evoked Potentials in the Rat

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