ABSTRACT
Neurophysiological studies in monkeys suggest selective representation of behaviourally relevant information in working memory. So far, no behavioural evidence for this has been reported for humans. Here, we investigated the role of behavioural relevance for access to human visuospatial working memory by using delayed oculomotor response tasks. Subjects were presented two successive visual cues in different and unpredictable locations while fixating on a central fixation point. After a delay, an unpredictable auditory signal (one beep or two beeps) sounded and the central fixation point was turned off, initiating the oculomotor response (i.e. memory-guided saccade) phase. Two groups of 10 subjects each were studied in two conditions: in the 'relevant' condition, subjects were instructed to memorize both visual cues and to move the eyes to the remembered position of the first cue (one beep) or the second cue (two beeps). The same stimuli were used in the 'irrelevant' condition, but subjects were instructed to memorize and move the eyes to the position of the first cue only, regardless of the second cue and the auditory signal. In the 'relevant' condition, we found a significant increase in errors of memory-guided saccades to the first cue, when the second cue was located between central fixation point and first cue. This spatially selective interference effect disappeared in the 'irrelevant' condition, despite identical stimuli. On a behavioural level, these results show for the first time the significance of behavioural relevance for access to human spatial working memory. These findings complement recent single-neuron studies in monkeys, showing that the neuronal substrates of working memory selectively represent behaviourally relevant perceptual information.
Subject(s)
Behavior/physiology , Memory, Short-Term/physiology , Saccades/physiology , Space Perception/physiology , Adult , Attention/physiology , Female , Humans , Male , Photic Stimulation , Psychomotor Performance/physiology , Reaction Time/physiologyABSTRACT
Anatomical studies in monkeys, and functional imaging and lesion studies in humans, suggest that, within the primate medial temporal neocortex, the parahippocampal cortex (PHC) is particularly involved in spatial tasks. However, evidence for a functional specialization of the PHC regarding its spatial memory functions has so far been lacking. Here, we investigated spatial memory functions of the human perirhinal cortex (PRC) and PHC. Patients with lesions affecting the PRC but sparing the PHC, and patients with lesions affecting both PRC and PHC, performed an oculomotor delayed response task with unpredictably varied memory delays of up to 30 s. Compared to controls, patients with PRC+PHC lesions showed a significant delay-dependent inaccuracy of memory-guided eye movements contralateral to the lesion side, whereas patients with PRC lesions showed no significant inaccuracy. Our results show that the PHC is a critical component for spatial memory in humans and suggest that (i) extrahippocampal spatial memory functions of the medial temporal lobe may not be equally distributed in the medial temporal neocortex, but may be largely confined to the PHC, and (ii) damage to connections between cortices involved in spatial cognition and rostral regions of the temporal lobe is unlikely to account for the observed spatial memory deficits with PHC lesions.
Subject(s)
Brain Diseases/physiopathology , Brain Diseases/psychology , Memory Disorders/etiology , Parahippocampal Gyrus/physiopathology , Space Perception/physiology , Adult , Brain Diseases/diagnosis , Female , Humans , Magnetic Resonance Imaging , Male , Memory/physiology , Reference Values , Saccades/physiologyABSTRACT
Behavioral studies in monkeys and humans suggest that systematic and variable errors of memory-guided saccades reflect distinct neuronal computations in primate spatial memory. We recorded memory-guided saccades with a 2-s delay in three patients with unilateral ischemic lesions of the frontal eye field and in three patients with unilateral ischemic lesions of the frontal eye field and the dorsolateral prefrontal cortex. Results suggest that systematic errors of memory-guided saccades originate in the frontal eye field and variable errors in the dorsolateral prefrontal cortex. These data are the first human lesion data to support the hypothesis that these regions provide functionally distinct contributions to spatial short-term memory.
Subject(s)
Memory/physiology , Prefrontal Cortex/physiology , Saccades/physiology , Visual Fields/physiology , Adult , Humans , Male , Middle Aged , Reproducibility of ResultsABSTRACT
The role of the caudate nucleus in ocular motor control is not well determined in humans. Eye movements were recorded from a 45 year old man with infarctions involving bilaterally the body of the caudate nucleus, with a greater extent on the left side. The patient exhibited a pattern of eye movement abnormalities in which a delay dependent decrease of accuracy of memory guided saccades predominated. By contrast, memory guided pointing was normal. It is concluded that the body of the caudate nucleus participates in a spatial short term memory network devoted to eye movements.
Subject(s)
Caudate Nucleus/pathology , Ischemic Attack, Transient/complications , Putamen/pathology , Saccades , Adult , Humans , Hypertension/complications , Ischemic Attack, Transient/diagnosis , Ischemic Attack, Transient/physiopathology , Magnetic Resonance Imaging , Male , Memory , Middle Aged , Reaction TimeABSTRACT
Lesion studies in monkeys suggest that neocortical subregions of the medial temporal lobe (MTL) carry memory functions independent of the hippocampal formation. The present study investigates possible differential contributions of MTL subregions to spatial memory in humans. Eye movements toward remembered spatial cues (memory-guided saccades) with unpredictably varied memorization delays of up to 30 seconds were recorded in patients with postsurgical lesions of the right MTL, either restricted to the hippocampal formation (n = 3) or including the adjacent neocortex (n = 5) and in 10 controls. Although saccadic targeting errors of patients with selective hippocampal lesions did not differ from controls, saccadic targeting errors of patients with additional neocortical involvement showed a significant and contralaterally pronounced increase at memorization delays above 20 seconds. We conclude that the human medial temporal neocortex carries spatial memory functions independent of the hippocampal formation and distinct from spatial short-term memory.
Subject(s)
Memory Disorders/pathology , Memory Disorders/physiopathology , Adult , Brain Mapping , Electrooculography , Eye Movements/physiology , Female , Hippocampus/physiopathology , Humans , Magnetic Resonance Imaging , Male , Space PerceptionABSTRACT
The contribution of extraocular muscle (EOM) proprioception to the eye position signal used to transform retinotopic visual information to a craniotopic reference frame remains uncertain. In this study we examined the effects of unilateral and bilateral proprioceptive deafferentation of the EOMs on the accuracy of reaching movements directed to visual targets. No significant changes occurred in the mean accuracy (constant error) or variance (variable error) of pointing after unilateral or bilateral deafferentation. We concluded that in normal animals efference copy provides sufficient information about orbital eye position to code space in craniotopic coordinates.
Subject(s)
Arm/physiology , Eye Movements/physiology , Psychomotor Performance/physiology , Animals , Conditioning, Psychological/physiology , Denervation , Macaca mulatta , Motor Neurons/physiology , Neurons, Afferent/physiology , Proprioception/physiologyABSTRACT
1. The function of extraocular muscle proprioception in the control of eye movements is uncertain. We tested the hypothesis that proprioception contributes to the long-term regulation of ocular alignment and eye movement conjugacy. 2. Eye movements were recorded in monkeys with unilateral extraocular muscle palsies, before and after proprioceptive deafferentation of the paretic eye. Following deafferentation, ocular alignment and saccade conjugacy gradually worsened over several weeks. In contrast, disconjugate adaptation induced by habitual binocular viewing with a prism (disparity-mediated adaptation) occurred normally after deafferentation. 3. These results provide the first evidence that proprioception functions in the control of eye movements in primates, and indicate that proprioception contributes to the long-term adaptive mechanisms that regulate ocular alignment during fixation and saccades. The error signal used in this process may be derived from a mismatch between the efference copy and proprioceptive afference.