Brenda Milner

LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS

In 1954 Scoville described a grave loss of recent memory which he had observed as a sequel to bilateral medial temporal-lobe resection in one psychotic patient and one patient with intractable seizures. In both cases the operations had been radical ones, undertaken only when more conservative forms of treatment had failed. The removals extended posteriorly along the mesial surface of the temporal lobes for a distance of approximately 8 cm. from the temporal tips and probably destroyed the anterior two-thirds of the hippocampus and hippocampal gyrus bilaterally, as well as the uncus and amygdala. The unexpected and persistent memory deficit which resulted seemed to us to merit further investigation. We have therefore carried out formal memory and intelligence testing of these two patients and also of eight other patients who had undergone similar, but less radical, bilateral medial temporallobe resections.* The present paper gives the results of these studies which point to the importance of the hippocampal complex for normal memory function. Whenever the hippocampus and hippocampal gyrus were damaged bilaterally in these operations some memory deficit was found, but not otherwise. We have chosen to report these findings in full, partly for their theoretical significance, and partly as a warning to others of the risk to memory involved in bilateral surgical lesions of the hippocampal region.

THE ROLE OF EARLY LEFT‐BRAIN INJURY IN DETERMINING LATERALIZATION OF CEREBRAL SPEECH FUNCTIONS

Preparatory to craniotomy for the relief of medically refractory focal epilepsy, the lateralization of cerebral speech functions was determined by the Wada intracarotid Amytal test in 134 patients with clinical and radiologic evidence of an early left-hemisphere lesion. Their results were compared with those for 262 patients (140 right-handed, 122 left-handed), who were tested in a similar way. One-third of the patients with early lesions were still right-handed, and 81% of these right-handers were left-hemisphere dominant for speech. In the non-right-handers, speech was represented in the left cerebral hemisphere in nearly a third of the group, in the right hemisphere in half the group, and bilaterally in the remainder. Bilateral speech representation was demonstrated in 15% of the non-right-handers without early left-brain injury and in 19% of those with evidence of such early injury, whereas it was extremely rare in the right-handed groups. In addition, nearly half the patients with bilateral speech representation exhibited a complete or partial dissociation between errors of naming and errors in the repetition of verbal sequences after Amytal injection into left or right hemispheres. This points to the possibility of a functionally asymmetric participation of the two hemispheres in the language processes of some normal left-handers. The results of the Amytal speech tests in this series of patients point to locus of lesion as one of the critical determinants in the lateralization of cerebral speech processes after early left-brain injury. It is argued that in such cases the continuing dominance of the left hemisphere for speech in largely contingent upon the integrity of the frontal and parietal speech zones.

Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. ☆

Abstract The report attempts to delineate certain residual learning capacities of H.M., a young man who became amnesic in 1953 following a bilateral removal in the hippocampal zone. In addition to being able to acquire new motor skills (C ORKIN [2]), this patient shows some evidence of perceptual learning. He also achieves some retention of very simple visual and tactual mazes in which the sequence of required turns is short enough to fit into his immediate memory span; even then, the rate of acquisition is extremely slow. These vestigial abilies, which have their occasional parallels in the patients everyday life, are assessed against the background of his continuing profound amnesia for most on-going events, an amnesia that persists in spite of above-average intelligence and superior performance on many perceptual tasks.

Visual recognition and recall after right temporal-lobe excision in man

Abstract A further effort was made to determine the effects of right anterior temporal lobectomy in man on visual perception and visual memory. Groups of patients with cortical resections from right or left temporal, frontal, or parietal regions were required to recognize photographs of faces within a larger array, after having been shown the faces previously. Three variations of this task were used: in the first, the interval between initial presentation and recognition test was filled with an irrelevant visual task. In the second, the delay remained but the interpolated task was omitted. In the third, there was only minimal delay (“immediate recognition”). On the first two tasks, patients with right temporal-lobe lesions had marked deficits compared with all other groups, but on the third task (minimal delay) no clearcut group differences were seen, because the normal control group did worse than with delay. Normal subjects (unlike patients with right temporal-lobe excisions) apparently use the delay period to consolidate and possibly recode their visual impressions. In the context of other tasks sensitive to right temporal-lobe lesions, the findings suggest a mild impairment in the perception of complex patterns after right anterior temporal lobectomy, and a much more severe one in the retention of the perceived material.

The role of the right hippocampus in the recall of spatial location

Abstract Patients with left or right temporal lobectomies, the amnesic patient H.M. with bilateral mesial temporal-lobe damage, and normal control subjects were tested on the incidental recall of objects and their location, both immediately and after a delay. An impairment was seen for both temporal-lobe groups in the delayed recall of objects, but only for the right temporal-lobe group in immediate and delayed recall of location. The deficits after right temporal lobectomy were contingent upon radical excision of the hippocampal region. On both object-recall and location-recall, H.M. was inferior to the most impaired patients with unilateral temporal lobectomies.

Design fluency: The invention of nonsense drawings after focal cortical lesions

Abstract One hundred patients with unilateral cortical excisions and 34 normal control subjects were tested for the ability to produce abstract (meaningless) designs under a time constraint. It was predicted that the task, testing fluency in a nonverbal mode, would tap the specialized abilities of anterior parts of the right hemisphere just as certain tests of word fluency tap those of the left frontal lobe. Results showed patients with right frontal and right fronto-central lesions to be the most impaired, with milder deficits being found in left frontal and right temporal groups, thus emphasizing the importance of both side and site of lesion in performance of this task.

VISUALLY-GUIDED MAZE LEARNING IN MAN: EFFECTS OF BILATERAL HIPPOCAMPAL, BILATERAL FRONTAL, AND UNILATERAL CEREBRAL LESIONS

Seventy-nine patients with different cerebral lesions were trained on a visually- guided stylus maze. The main findings were: (1) bilateral hippocampal lesions produced the most severe impairment, with one patient showing no progress in 215 trials; (2) right temporal lobectomy produced a significant deficit, particularly when the underlying hippocampus was radically excised, whereas patients with left temporal-lobe lesions of equal extent, or with small parietal-lobe lesions of either hemisphere, obtained normal scores; (3) larger lesions of frontal or right posterior cortex severely impaired maze learning, suggesting that size as well as locus of cortical lesion may be a factor in maze-performance; (4) only frontal-lobe lesions affected the ability to follow test instructions.

Behavioural effects of frontal-lobe lesions in man

The study of patients with excisions from the frontal lobes has revealed specific cognitive deficits that appear against a background of normal functioning on a variety of perceptual and memory tasks, as well as on conventional intelligence tests. These deficits include a reduced output on fluency tasks, faulty regulation of behaviour of external cues, and impaired organization and monitoring of material to be remembered, and of the subjects own responses. Differential effects related to the side of the lesion are less consistently observed after frontal-than after temporal-lobe excisions. Such effects, when they do occur, may depend as much on the demands of the task as on the nature of the test material.

Lateralized suppression of dichotically presented digits after commissural section in man.

Right-handed patients with surgical disconnection of the cerebral hemispheres cannot report verbal input to the left ear if diferent verbal stimuli have been channeled simultaneously to the right ear. With monaural stimulation, they show equal accuracy of report for the two ears. These findings highlight the dominance of the contralateral over the ipsilateral auditory projection system. Suppression of right-ear input is obtained in nonverbal tests. Dissociation between verbal and left-hand stereognostic responses indicate a right-left dichotomy for auditory experience in the disconnected hemispheres.

Frontal-lobe contribution to recency judgements

Three recency-discrimination tasks (involving concrete words, representational drawings and abstract paintings) were administered to 117 patients who had undergone unilateral cortical removals, and to 20 normal control subjects. Frontal or anterior temporal-lobe excision did not impair simple item recognition, and neither left nor right anterior-temporal lobectomy affected recency judgements on any task. In contrast, excisions that encroached on the mid-lateral frontal cortex impaired verbal recency judgements, the deficit being mild after right frontal lobectomy. Patients with right frontal-lobe removals showed the greatest impairment in recency discrimination on the two pictorial tests. The results provide evidence for hemispheric specialization related to the nature of the stimulus material and some support for a functional role for the left mid-lateral frontal cortex in verbal recency judgements.