0
July 1960, Vol 3, No. 1 >
Article | July 1960

Hippocampal Slow Waves: Title and subTitle BreakDistribution and Phase Relationships in the Course of Approach Learning

W. R. ADEY, M.D.; C. W. DUNLOP, Ph.D.; C. E. HENDRIX, M.S.
[+] Author Affiliations

Accepted for publication Jan. 18, 1960.

This work was assisted by Grants B-610, B-611, and B-1883 from the National Institutes of Health of the U.S. Public Health Service, and by a grant from the Ford Foundation.


Arch Neurol. 1960;3(1):74-90. doi:10.1001/archneur.1960.00450010074007
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Comments

The functions of the temporal lobe, and its preponderant role in the integrative aspects of social behavior, are well known (Bucy and Klüver,13 1939) and have been the subject of recent reviews (Adey,2 1959; Baldwin and Bailey,8 1958). To some extent, physiological dissection of the picture of "psychic blindness" characterizing the complete bilateral temporal lobectomy has been possible with more limited resections, with aspects of hypersexuality, loss of memory, taming, and exaggerated rage responses, each reported as the dominant aspect of a variety of limited resections in man and animals (Adey,1 1958; Bard and Mountcastle,10 1948; Green, Clemente, and de Groot,24 1958; Schreiner and Kling,45 1953; Scoville and Milner,46 1957).

Historically, the limbic lobe, set as a ring of cortex at the medial margin of the hemisphere, has been described as a somatic integrating center concerned with the integration of somatic influxes

REFERENCES

1 +
Adey, W. R.:  Organization of the Rhinencephalon , in Reticular Formation of the Brain , edited by H. H. Jasper, L. D. Proctor, R. S. Knighton, W. C. Noshay, and R. T. Costello, Boston, Little, Brown & Company, 1958;.
2 +
Adey, W. R.:  Recent Studies of the Rhinencephalon in Relation to Temporal Lobe Epilepsy and Behavior Disorders , Internat. Rev. Neurobiol. 1:1-46, 1959;.
3 +
Adey, W. R.; Carter, I. D., and Porter, R.:  Temporal Dispersion in Cortical Response , J. Neurophysiol. 17:167-182, 1954;.
4 +
Adey, W. R.; Dunlop, C. W., and Sunderland, S.:  A Survey of Rhinencephalic Interconnections with the Brain Stem , J. Comp. Neurol. 110:173-204, 1958;.
5 +
Adey, W. R., and Meyer, M.:  Hippocampal and Hypothalamic Connections of the Temporal Lobe in the Monkey , Brain 75:358-384, 1952;.
6 +
Adey, W. R.; Porter, R., and Carter, I. D.:  Temporal Dispersion in Cortical Afferent Volleys as Factor in Perception: Evoked Potential Study of Deep Somatic Sensibility in the Monkey , Brain 77:325-344, 1954;.
7 +
Adey, W. R.; Sunderland, S., and Dunlop, C. W.:  The Entorhinal Area: Electrophysiological Studies of Its Interrelations with the Rhinencephalon and the Brain Stem , Electroencephalog. & Clin. Neurophysiol. 9:309-324, 1957;.
8 +
Baldwin, M., and Bailey, P.: Temporal Lobe Epilepsy , Springfield, Ill., Charles C Thomas, Publisher, 1958;.
9 +
Bendat, J. S.: Principles and Applications of Random Noise Theory , New York, John Wiley & Sons, Inc., 1958;, Chap. 7.
10 +
Bard, P., and Mountcastle, V.:  Some Forebrain Mechanisms Involved in the Expression of Rage with Special Reference to the Suppression of Angry Behaviour , A. Res. Nerv. & Ment. Dis. Proc. (1947) 27:362-404, 1948;.
11 +
Brazier, M. A. B., and Barlow, J. S.:  Some Applications of Correlation Analysis to Clinical Problems in Electroencephalography , Electroencephalog. & Clin. Neurophysiol. 8:325-331, 1956;.
12 +
Broca, P.:  Anatomie comparée des circonvolutions cérébrales: Le grand lobe limbique dans la série des mammiféres , Rev. anthrop. 1:385-406, 1878;.
13 +
Bucy, P., and Klüver, H.:  Anatomic Changes Secondary to Temporal Lobectomy , Arch. Neurol. & Psychiat. 44:1142-1146, 1940;.
14 +
Ramón y Cajal, S.: Histologie du systéme nerveux de l'homme et des vertébrés , Paris, A. Maloine, 1909;.
15 +
Cragg, B. G., and Hamlyn, L. H.:  Some Commissural and Septal Connections of the Hippocampus in the Rabbit: A Combined Histological and Electrical Study , J. Physiol. 135:460-485, 1957;.
16 +
Dunlop, C. W.; Adey, W. R.; Killam, K. F., and Brazier, M. A. B.:  Effects of Gamma-Aminobutyric Acid and Thiosemicarbazide on Cerebellar Activity in the Cat , Fed. Proc. 18:38, 1959;.
17 +
Elliot Smith, G.:  Some Problems Relating to the Evolution of the Brain: The Arris and Gale Lectures , Lancet 1:1-11, 147-153, 221-227, 1910;.
18 +
von Euler, C.; Green, J. D., and Ricci, G.:  The Role of Hippocampal Dendrites in Evoked Responses and After-Discharges , Acta physiol. scandinav. 42:87-111, 1958;.
19 +
Freeman, W.:  Prepyriform Electrical Activity Associated with Drive , Physiologist 1 ( (Pt. 4) ):23-24, 1958;.
20 +
Fuller, J. L.; Rosvold, H. E., and Pribram, K. A.:  The Effect on Affective and Cognitive Behavior in the Dog of Lesions of the Pyriform-Amygdala-Hippocampal Complex , J. Comp. Physiol. & Psychol. 50:89-96, 1957;.
21 +
Grastyán, E.; Lissák, K.; Madarász, I., and Donhoffer, H.:  Hippocampal Electrical Activity During the Development of Conditioned Reflexes , Electroencephalog. & Clin. Neurophysiol. 11:409-430, 1959;.
22 +
Green, J. D., and Adey, W. R.:  Electrophysiological Studies of Hippocampal Connections and Excitability , Electroencephalog. & Clin. Neurophysiol. 8:245-262, 1956;.
23 +
Green, J. D., and Arduini, A.:  Hippocampal Electrical Activity in Arousal , J. Neurophysiol. 17:533-557, 1954;.
24 +
Green, J. D.; Clemente, C. D., and de Groot, J.:  Rhinencephalic Lesions and Behavior in Cats , J. Comp. Neurol. 108:505-536, 1957;.
25 +
Green, J. D., and Machne, X.:  Unit Activity of Rabbit Hippocampus , Am. J. Physiol. 181:219-224, 1955;.
26 +
Herrick, C. J.:  The Functions of the Olfactory Parts of the Cerebral Cortex , Proc. Nat. Acad. Sc. 19:7-14, 1933;.
27 +
Hess, E.:  Imprinting, an Effect of Early Experience: Imprinting Determines Later Social Behavior in Animals , Science 130:133-141, 1959;.
28 +
Holmes, J. E., and Adey, W. R.:  Electrical Activity of the Entorhinal Cortex During Conditioned Behavior , Physiologist 2 ( (Pt. 3) ):60, 1959;.
29 +
Jasper, H. H., and Rasmussen, T.:  Studies of Clinical and Electrical Responses to Deep Temporal Stimulation in Men with Some Considerations of Functional Anatomy , A. Res. Nerv. & Ment. Dis. Proc. (1957) , 36:316-334, 1958;.
30 +
Jung, R., and Kornmüller, A. E.:  Eine Methodik der Ableitung lokalisierter Potential-schwankungen aus subcorticalen Hirngebieten , Arch. Psychiat. 109:1-30, 1939;.
31 +
Konorski, J., Editor: Conditioned Reflexes and Neuron Organization , translated from the Polish ms. by S. Garry, Cambridge Biological Studies, General Editors, C. H. Waddington, London, Cambridge University Press, 1948;, pp. 78-79.
32 +
Lee, Y. W.: Application of Statistical Methods to Communication Problems , Massachusetts Institute of Technology Research Laboratory of Electronics Report 181, 1950;.
33 +
Lesse, H.:  Electrographic Recordings of Amygdaloid Activity During a Conditioned Response , Fed. Proc. 16:343, 1957;.
34 +
Li, C. L.; McLennan, H., and Jasper, H.:  Brain Waves and Unit Discharge in Cerebral Cortex , Science 116:656-657, 1952;.
35 +
Lorente de Nó, R.:  Studies on the Structures of the Cerebral Cortex: I. The Area Entorhinalis , J. Psychol. u. Neurol. 45:381-438, 1933;.
36 +
Lorente de Nó, R.:  Studies on the Structure of the Cerebral Cortex: II. Continuation of the Study of the Ammonic System , J. Psychol. u. Neurol. 46:113-177, 1934;.
37 +
Maclean, P. D.:  The Limbic System ("Visceral Brain") in Relation to Central Gray and Reticulum of the Brain Stem: Evidence of Interdependence in Emotional Processes , Psychosom. Med. 17:355-366, 1955;.
38 +
Maclean, P. D.:  Chemical and Electrical Stimulation of Hippocampus in Unrestrained Animals , A.M.A. Arch. Neurol. & Psychiat. 78:113-142, 1957;.
39 +
McLardy, T.:  Hippocampal Formation of Brain as a Detector-Coder of Temporal Patterns of Information , Perspectives Biol. & Med. 2:443-452, 1959;.
40 +
Morin, F.:  An Experimental Study of Hypothalamic Connections in the Guinea Pig , J. Comp. Neurol. 92:193-213, 1950;.
41 +
Papez, J. W.:  A Proposed Mechanism of Emotion , Arch. Neurol. & Psychiat. 38:725-743, 1937;.
42 +
Pribram, K. H., and Mishkin, M.:  Simultaneous and Successive Visual Discrimination by Monkeys with Inferotemporal Lesions , J. Comp. & Physiol. Psychol. 48:198-202, 1955;.
43 +
Renshaw, B.; Forbes, A., and Morison, B. R.:  Activity of Isocortex and Hippocampus: Electrical Studies with Micro-Electrodes , J. Neurophysiol. 3:74-105, 1940;.
44 +
Rosvold, H. E., and Mishkin, M.: Nonsensory Effects of Frontal Lesions on Performance of Discrimination Tasks, delivered at UNESCO Symposium on Brain Mechanisms and Learning, Montevideo, August, 1959.
45 +
Schreiner, L., and Kling, A.:  Behavioral Changes Following Rhinencephalic Injury in Cat , J. Neurophysiol. 16:643-659, 1953;.
46 +
Scoville, W. B., and Milner, B.:  Loss of Recent Memory After Bilateral Hippocampal Lesions , J. Neurol. Neurosurg. & Psychiat. 20:11-21, 1957;.
47 +
Shannon, C. E.:  Communication in the Presence of Noise , Proc. Inst. Radio Engin. 37:10-21, 1949;.
48 +
Wiener, N.:  Generalized Harmonic Analysis , Acta math . 55:117-258, 1930;.

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1 +
Adey, W. R.:  Organization of the Rhinencephalon , in Reticular Formation of the Brain , edited by H. H. Jasper, L. D. Proctor, R. S. Knighton, W. C. Noshay, and R. T. Costello, Boston, Little, Brown & Company, 1958;.
2 +
Adey, W. R.:  Recent Studies of the Rhinencephalon in Relation to Temporal Lobe Epilepsy and Behavior Disorders , Internat. Rev. Neurobiol. 1:1-46, 1959;.
3 +
Adey, W. R.; Carter, I. D., and Porter, R.:  Temporal Dispersion in Cortical Response , J. Neurophysiol. 17:167-182, 1954;.
4 +
Adey, W. R.; Dunlop, C. W., and Sunderland, S.:  A Survey of Rhinencephalic Interconnections with the Brain Stem , J. Comp. Neurol. 110:173-204, 1958;.
5 +
Adey, W. R., and Meyer, M.:  Hippocampal and Hypothalamic Connections of the Temporal Lobe in the Monkey , Brain 75:358-384, 1952;.
6 +
Adey, W. R.; Porter, R., and Carter, I. D.:  Temporal Dispersion in Cortical Afferent Volleys as Factor in Perception: Evoked Potential Study of Deep Somatic Sensibility in the Monkey , Brain 77:325-344, 1954;.
7 +
Adey, W. R.; Sunderland, S., and Dunlop, C. W.:  The Entorhinal Area: Electrophysiological Studies of Its Interrelations with the Rhinencephalon and the Brain Stem , Electroencephalog. & Clin. Neurophysiol. 9:309-324, 1957;.
8 +
Baldwin, M., and Bailey, P.: Temporal Lobe Epilepsy , Springfield, Ill., Charles C Thomas, Publisher, 1958;.
9 +
Bendat, J. S.: Principles and Applications of Random Noise Theory , New York, John Wiley & Sons, Inc., 1958;, Chap. 7.
10 +
Bard, P., and Mountcastle, V.:  Some Forebrain Mechanisms Involved in the Expression of Rage with Special Reference to the Suppression of Angry Behaviour , A. Res. Nerv. & Ment. Dis. Proc. (1947) 27:362-404, 1948;.
11 +
Brazier, M. A. B., and Barlow, J. S.:  Some Applications of Correlation Analysis to Clinical Problems in Electroencephalography , Electroencephalog. & Clin. Neurophysiol. 8:325-331, 1956;.
12 +
Broca, P.:  Anatomie comparée des circonvolutions cérébrales: Le grand lobe limbique dans la série des mammiféres , Rev. anthrop. 1:385-406, 1878;.
13 +
Bucy, P., and Klüver, H.:  Anatomic Changes Secondary to Temporal Lobectomy , Arch. Neurol. & Psychiat. 44:1142-1146, 1940;.
14 +
Ramón y Cajal, S.: Histologie du systéme nerveux de l'homme et des vertébrés , Paris, A. Maloine, 1909;.
15 +
Cragg, B. G., and Hamlyn, L. H.:  Some Commissural and Septal Connections of the Hippocampus in the Rabbit: A Combined Histological and Electrical Study , J. Physiol. 135:460-485, 1957;.
16 +
Dunlop, C. W.; Adey, W. R.; Killam, K. F., and Brazier, M. A. B.:  Effects of Gamma-Aminobutyric Acid and Thiosemicarbazide on Cerebellar Activity in the Cat , Fed. Proc. 18:38, 1959;.
17 +
Elliot Smith, G.:  Some Problems Relating to the Evolution of the Brain: The Arris and Gale Lectures , Lancet 1:1-11, 147-153, 221-227, 1910;.
18 +
von Euler, C.; Green, J. D., and Ricci, G.:  The Role of Hippocampal Dendrites in Evoked Responses and After-Discharges , Acta physiol. scandinav. 42:87-111, 1958;.
19 +
Freeman, W.:  Prepyriform Electrical Activity Associated with Drive , Physiologist 1 ( (Pt. 4) ):23-24, 1958;.
20 +
Fuller, J. L.; Rosvold, H. E., and Pribram, K. A.:  The Effect on Affective and Cognitive Behavior in the Dog of Lesions of the Pyriform-Amygdala-Hippocampal Complex , J. Comp. Physiol. & Psychol. 50:89-96, 1957;.
21 +
Grastyán, E.; Lissák, K.; Madarász, I., and Donhoffer, H.:  Hippocampal Electrical Activity During the Development of Conditioned Reflexes , Electroencephalog. & Clin. Neurophysiol. 11:409-430, 1959;.
22 +
Green, J. D., and Adey, W. R.:  Electrophysiological Studies of Hippocampal Connections and Excitability , Electroencephalog. & Clin. Neurophysiol. 8:245-262, 1956;.
23 +
Green, J. D., and Arduini, A.:  Hippocampal Electrical Activity in Arousal , J. Neurophysiol. 17:533-557, 1954;.
24 +
Green, J. D.; Clemente, C. D., and de Groot, J.:  Rhinencephalic Lesions and Behavior in Cats , J. Comp. Neurol. 108:505-536, 1957;.
25 +
Green, J. D., and Machne, X.:  Unit Activity of Rabbit Hippocampus , Am. J. Physiol. 181:219-224, 1955;.
26 +
Herrick, C. J.:  The Functions of the Olfactory Parts of the Cerebral Cortex , Proc. Nat. Acad. Sc. 19:7-14, 1933;.
27 +
Hess, E.:  Imprinting, an Effect of Early Experience: Imprinting Determines Later Social Behavior in Animals , Science 130:133-141, 1959;.
28 +
Holmes, J. E., and Adey, W. R.:  Electrical Activity of the Entorhinal Cortex During Conditioned Behavior , Physiologist 2 ( (Pt. 3) ):60, 1959;.
29 +
Jasper, H. H., and Rasmussen, T.:  Studies of Clinical and Electrical Responses to Deep Temporal Stimulation in Men with Some Considerations of Functional Anatomy , A. Res. Nerv. & Ment. Dis. Proc. (1957) , 36:316-334, 1958;.
30 +
Jung, R., and Kornmüller, A. E.:  Eine Methodik der Ableitung lokalisierter Potential-schwankungen aus subcorticalen Hirngebieten , Arch. Psychiat. 109:1-30, 1939;.
31 +
Konorski, J., Editor: Conditioned Reflexes and Neuron Organization , translated from the Polish ms. by S. Garry, Cambridge Biological Studies, General Editors, C. H. Waddington, London, Cambridge University Press, 1948;, pp. 78-79.
32 +
Lee, Y. W.: Application of Statistical Methods to Communication Problems , Massachusetts Institute of Technology Research Laboratory of Electronics Report 181, 1950;.
33 +
Lesse, H.:  Electrographic Recordings of Amygdaloid Activity During a Conditioned Response , Fed. Proc. 16:343, 1957;.
34 +
Li, C. L.; McLennan, H., and Jasper, H.:  Brain Waves and Unit Discharge in Cerebral Cortex , Science 116:656-657, 1952;.
35 +
Lorente de Nó, R.:  Studies on the Structures of the Cerebral Cortex: I. The Area Entorhinalis , J. Psychol. u. Neurol. 45:381-438, 1933;.
36 +
Lorente de Nó, R.:  Studies on the Structure of the Cerebral Cortex: II. Continuation of the Study of the Ammonic System , J. Psychol. u. Neurol. 46:113-177, 1934;.
37 +
Maclean, P. D.:  The Limbic System ("Visceral Brain") in Relation to Central Gray and Reticulum of the Brain Stem: Evidence of Interdependence in Emotional Processes , Psychosom. Med. 17:355-366, 1955;.
38 +
Maclean, P. D.:  Chemical and Electrical Stimulation of Hippocampus in Unrestrained Animals , A.M.A. Arch. Neurol. & Psychiat. 78:113-142, 1957;.
39 +
McLardy, T.:  Hippocampal Formation of Brain as a Detector-Coder of Temporal Patterns of Information , Perspectives Biol. & Med. 2:443-452, 1959;.
40 +
Morin, F.:  An Experimental Study of Hypothalamic Connections in the Guinea Pig , J. Comp. Neurol. 92:193-213, 1950;.
41 +
Papez, J. W.:  A Proposed Mechanism of Emotion , Arch. Neurol. & Psychiat. 38:725-743, 1937;.
42 +
Pribram, K. H., and Mishkin, M.:  Simultaneous and Successive Visual Discrimination by Monkeys with Inferotemporal Lesions , J. Comp. & Physiol. Psychol. 48:198-202, 1955;.
43 +
Renshaw, B.; Forbes, A., and Morison, B. R.:  Activity of Isocortex and Hippocampus: Electrical Studies with Micro-Electrodes , J. Neurophysiol. 3:74-105, 1940;.
44 +
Rosvold, H. E., and Mishkin, M.: Nonsensory Effects of Frontal Lesions on Performance of Discrimination Tasks, delivered at UNESCO Symposium on Brain Mechanisms and Learning, Montevideo, August, 1959.
45 +
Schreiner, L., and Kling, A.:  Behavioral Changes Following Rhinencephalic Injury in Cat , J. Neurophysiol. 16:643-659, 1953;.
46 +
Scoville, W. B., and Milner, B.:  Loss of Recent Memory After Bilateral Hippocampal Lesions , J. Neurol. Neurosurg. & Psychiat. 20:11-21, 1957;.
47 +
Shannon, C. E.:  Communication in the Presence of Noise , Proc. Inst. Radio Engin. 37:10-21, 1949;.
48 +
Wiener, N.:  Generalized Harmonic Analysis , Acta math . 55:117-258, 1930;.

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