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Latencies of visually responsive neurons in various regions of the rhesus monkey brain and their relation to human visual responses
Biological Psychology North-Holland
111
26 (1988) 111-116
LATENCIES OF VISUALLY RESPONSIVE NEURONS IN VARIOUS REGIONS OF THE RHESUS MONKEY BRAIN AND THEIR RELATION TO HUMAN VISUAL RESPONSES * David Lee ROBINSON Laboratory of Sensorimotor
Research, National Eye Institute, Bethesda, MD 20892, U.S.A.
Michael D. RUGG MRC Cognitive Neuroscience Research Group, University of St Andrews, Fife KY16 9JU, U.K.
St Andrews,
The temporal characteristics of visually responsive neurons in a variety of areas of the monkey brain are presented. These data allow a comparison to be made between the latencies of components of the human visual ERP, and the onset latencies of neurons in regions which are candidate sources of these ERP phenomena.
1. Introduction An important aspect of research using human event-related potentials (ERPs) is the identification of the brain structures responsible for the generation and modulation of these scalp-recorded waveforms. Because of the difficulties inherent in inferring the cerebral origins of an ERP effect from its scalp distribution alone (e.g., Wood, 1982), it is desirable also to employ other physiological criteria when these are available. In this regard, consideration of relevant single neuron data from sub-human primates might sometimes help to narrow down the range of possible generators of a given ERP effect. This kind of reasoning has been employed, for example, by Hillyard, Munte and Neville (1985) in their analysis of ERPs in relation to visual-spatial attention. They argued that the sensitivity of the Pl component of the visual ERP to spatial attention was unlikely to reflect activity in areas 17 or 18 of the visual cortex, because single unit studies in monkeys had failed to find neurons in these areas sensitive to spatial attention. The good temporal resolution of scalp-recorded ERPs means that it is possible to compare ERP latencies with those found for changes in the firing * Reprint requests may be directed to either author. during the preparation of this paper.
0301-0511/88/$3.50
We are grateful
0 1988, Elsevier Science Publishers
to Dr V.H. Perry for advice
B.V. (North-Holland)
112
D.L. Robinson and M.D. Rugg / Onset latencies of visual responses
rates of single neurons in the brains of experimental animals. Such comparisons could provide a useful source of information about the possible cerebral origins of ERP components and their modulation, if it is assumed that the neural events generating scalp-recorded potentials are closely allied in time with changes in the activity of single neurons. To take an extreme, hypothetical example, it seems implausible to postulate that an ERP deflection with an onset of 300 ms directly reflects activity in a structure in which single neurons showed enhanced activity within 50 ms post-stimulus. Similarly, it would also seem unlikely that a brain area in which cells do not become active until 100 ms generates an ERP effect with an onset latency of 50 ms. The purpose of the present paper is to provide some information on the timing of visually-responsive neurons in various regions of the monkey brain, thereby allowing ERP researchers to compare their own data with those from relevant animal studies more easily than at present. The brain regions discussed include some which are thought to play a role in visual attention (pulvinar, posterior parietal cortex, area V4 and peri-frontal cortex), form vision (area 17, area 18, area V4 and inferotemporal cortex), and visually-guided eye-movements (superior colliculus and frontal eye fields), and we hope that these data will be of particular benefit to ERP researchers in these and related fields of research. Comparable data may also exist for the auditory and somatosensory systems.
2. Applicability of the data Except for values for the superior colliculus, the data in the present paper come from studies of awake rhesus monkeys. Since these animals are conscious and actively participating in many of the experimental tasks, it is likely that their behavioural states and neural processing would be comparable to human subjects of similar ERP experiments. Many studies have demonstrated that the visual and oculomotor capacities of the two species are remarkably similar (Bough, 1970; Carpenter, 1977; Cavonious & Robbins, 1973; DeValois, Morgan, Polson, Mead, & Hull, 1974; DeValois, Morgan, & Snodderly, 1974; Sarmiento, 1975). Therefore, although direct evidence is lacking, it is reasonable to suppose that the anatomy and function of the human and rhesus monkey visual systems are very similar (Cowey, 1982; Van Essen, 1985). Moreover, although the visual pathways are somewhat longer in humans than monkeys, the effects of this on relative conduction times in the two species is likely to be negligible given the limits of accuracy to which latency measurements can be made. Accordingly, we are assuming that the values derived from the monkey can be used as estimates for the human brain without adjustment.
D.L. Robinson and M.D. Rugg / Onset latencies of visual responses
113
3. The data The data are shown in table 1, and summarised in fig. 1. They consist mainly of the mean onset latencies of visually-responsive neurons in various regions of the brains of conscious monkeys. The onset latencies for individual cells were determined at the point of significant increment of a histogram based on several stimulus presentations. Where possible, the standard deviation and range of the onset latencies of the neurons sampled in a particular region are also presented. Since conduction times can differ for various parts of the visual field, we have also indicated whether the evoking stimuli were presented at fovea1 or extra-foveal locations. Several of the brain areas have been tested during various types of active visual behaviour, and we have noted
Table 1 Onset latencies (ms) of visually-responsive neurons in various areas of the rhesus monkey brain Area
Mean
Sub-cortex Superior Colliculus Pulvinar: Inferior Map Lateral Map Dorsomedial
64 84
Cortex Area 17 Area 18 V4 complex
53 c.d 67 c*d 78 a,c.d
44
66
b.c.d
b,c.d
a b ’ d ’
Range
Reference
_
34-60
Moors and Vendrick (1979)
16 20 48
b.c.d a.c.d
18 _
31 _
58
125 d,e
_ _
_
21 26
80 c.d Middle temporal area Inferotemporal area Superior temporal sulcus Posterior parietal (area 7) Frontal eye-fields (area 8) Peri-frontal cortex (area 46)
SD
70-220 a*c,d (60% < 120)
Petersen et al. (1985) Petersen et al. (1985) Petersen et al. (1985)
Maunsell (pew comm., fall 1987) Maunsell (pers. comm., fall 1987) Both and Fischer (1983) Maunsell (pers. comm., fall 1987) Maunsell (pers. comm., fall 1987) Richmond et al. 1983)
20
Perett et al. (1982)
90 a.c.d 87 b.c.d
31 35
Petersen et al. (1985) Goldberg and Bushnell (1981)
91
16
Both and Goldberg (1987)
a.c.d
Attentionally responsive. Eye-movement modulation. Non-fovea1 stimuli. Fovea1 stimuli. Neurons responsive to face stimuli.
114
D.L. Robinson and M.D. Rugg / Onsst latencies of visual responses POSTERIOR PARIETAL CORTEX (AREA 7) 90 MSEC
FRONTAL EYE FIELDS (AREA 81.
PERIPRINCIPAL CORT (AREA 48) -9l MSEi’
RIATE CORTEX (AREA 17)
PULVINAR’
IDDLE TEMPORAL CORTEX
PI 66 MSEC
58 MSEC
/ INFERIOR TEMPORAL CORTEX
coLLlcuws 44 MSEC
Fig. 1. Schematic view of the lateral surface of the rhesus monkey brain. Each line indicates the location on the brain of a visual area for which a latency has been determined. The brain is drawn as if part of the temporal lobe has been removed to expose the superior colliculus. The diagonally striped region on the temporal lobe represents the general region of the pulvinar nuclei.
whether neurons in each area responded in an attentionally selective fashion, that is whether any enhancement in their firing rates was dependent upon the evoking stimulus being presented within the focus of attention and whether the enhancement was independent of motor responses (Wurtz, Goldberg, & Robinson, 1980) I. Other areas are noted which contain cells selectively enhanced prior to visually-guided saccadic eye-movements.
4. Discussion
A number of points should be made about these data. Firstly, the absolute values should be treated with caution, as changes in such variables as stimulus brightness and retinal eccentricity alter the efficiency of visual processing and would be expected, therefore, to give rise to variations in neuronal onset latencies (Richmond, Optican, Podell, 8z Spitzer, 1987). This should not affect the relative onset latencies of different regions. Secondly, the values represent the beginning of activity and not the time of the most intense response. It is * With the exception of Richmond, Wurtz, and Sato (1983), all the studies noted in table 1 report attentionally selective neurons investigated with visual-spatial attention. Richmond et al. (1983) studied selectivity to different visual patterns presented at the same spatial locus.
D.L. Robinson and M.D. Rugg / Onset latencies of visual responses
115
possible that some stimuli or visual areas have gradual increases in firing whereas others may be more abrupt. Such differences might be expected to be reflected in human ERP onset latencies. Thirdly, changes in stimulus pattern can alter the qualitative nature of the response of an individual neuron. For example, one pattern can evoke a transient burst of activity whereas another visual pattern can elicit inhibition (fig. 9, Richmond et al., 1987). Fourthly, the data allow reasonably firm estimates about the shortest likely onset latency of an ERP effect that is to be attributed to a particular brain region. They do not, however, constrain estimates about the maximum acceptable latency to the same extent. Finally, single neurons vary in the duration of their response to visual stimuli. For some cortical cells there can be a sustained discharge for the duration of a stimulus presentation. For others, there can be a varied pattern of activity for the duration of the stimulus. For yet other cells there is only a transient burst at the onset and/or termination of an image (Richmond et al., 1987). Some cells alter these temporal response patterns with changes in the visual stimulus. In addition, some cortical neurons have sustained discharges which long outlast the brief stimulus which evokes them (Bruce & Goldberg, 1985, fig. 18). It is generally assumed that multiple visual areas subserve different visual functions in the realms of perception and visual behaviour (Van Essen, 1985). Consistent with this hypothesis is the observation that certain types of active behaviour can augment the responsiveness of cells in certain areas. Since in most areas the enhancement is almost simultaneous with the “on response”, this might be expected to increase the amplitude of an ERP effect but not its latency. In area V4 the attentional effects arise about 30 ms after the “on response” (Moran, 1985) and could well change the waveshape of the ERP. It is often assumed that ERPs to visual stimuli recorded at anterior sites are likely to reflect non-specific activity (e.g., NXatanen & Michie, 1979; Van Voorhis & Hillyard, 1977). However, the onset latencies of neurons in areas of frontal cortex implicated in visual processing are comparable with those in several posterior visual areas (e.g., frontal eye fields 87 ms; inferior parietal cortex 90 ms). Since the neural activity in these frontal regions may contribute to scalp-recorded ERPs, the anterior/posterior distribution of a visual ERP component may not be indicative of whether or not it reflects .brain activity specific to the visual modality.
References Both, R. & Fischer, B. (1983). Saccadic reaction times and activation of the prelunate cortex: Parallel observations in trained rhesus monkeys. Experimental Brain Research, 50, 201-210.
116
D. L. Robinson and M.D. Rugg / Onset latencies of visual responses
Both, R., L Goldberg, M.E. (1987). Saccade-related modulation of visual activity in monkey pre-frontal cortex. Investigative Ophthalmology and Visual Science, 28, 124. Bough, E.W. (1970). Stereoscopic vision in the macaque monkey: a behavioural demonstration. Nature, 225, 42-44. Bruce, C.J., & Goldberg, M.E. (1985). Primate frontal eye fields: I. Single neurons discharging before saccades. Journal of Neurophysiology, 53, 603-635. Carpenter, R.H.S. (1977). Movements of the eyes. London: Pion. Cavonious, CR., & Robbins, D.O. (1973). Relationships between luminance and visual acuity in the rhesus monkey. Journal of Physiology (London), 232, 239-246. Cowey, A. (1982). Sensory and non-sensory visual disorders in man and monkey. Philosophical Transactions of the Royal Sociev of London, B 298, 3-13. DeValois, R.L., Morgan, H.C., Polson, M.C., Mead, W.R., & Hull, E.M. (1974). Psychophysical studies of monkey vision: I. Macaque luminosity and color vision tests. Vision Research, 14, 53-67. DeValois, R.L., Morgan, H., & Snodderly, D.M. (1974). Psychophysical studies of monkey vision: III. Spatial luminance contrast sensitivity tests of macaque and human observers. Vision Research, 14, 75-81. Goldberg, M.E., & Bushnell, M.C. (1981). Behavioural enhancement of visual responses in monkey cerebral cortex: II. Modulation in frontal eye fields specifically related to saccades. Journal of Neurophysiology, 46, 773-787. Hillyard, S.A., Munte, T.F., & Neville, H.J. (1985). Visual-spatial attention, orienting and brain physiology. In M.I. Posner & O.S.M. Marin (Eds.), Attention andperformance XI (pp. 63-84). London: Lawrence Erlbaum. Moors, J., & Vendrick, A.J.H. (1979). Responses of single units in the monkey superior colliculus to stationary flashing stimuli. Experimental Brain Research, 35, 333-347. Moran, J.C. (1985). Selective attention gates the processing of visual information in primate extrastriate cortex. Unpublished PhD Thesis, Univeristy of Oregon. Nllt%nen, R., & Michie, P.T. (1979). Early selective-attention effects on the evoked potential: A critical review and reinterpretation. Biological Psychology, 8, 81-136. Perrett, D.I., Rolls, E.T., 65 Caan, W. @982). Visual neurones responsive to faces in the monkey temporal cortex. Experimental Brain Research, 47, 329-342. Petersen, S.E., Robinson, D.L., & Keys, W. (1985). Pulvinar nuclei of the behaving rhesus monkey: Visual responses and their modulation. Journal of Neurophysiology, 54, 867-886. Richmond, B.J., Optican, L.M., Podell, M., & Spitzer, H. (1987). Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex: I. Response characteristics. Journal of Neurophysiology, 57, 132-146. Richmond, B.J., Wurtz, R.H., & Sato, T. (1983). Visual responses of inferior temporal neurons in awake rhesus monkey. Journal of Neurophysiology, 50, 1415-1432. Sarmiento, R.F. (1975). The stereoacuity of macaque monkey. Vision Research, 15, 493-498. Van Essen, D.C. (1985). Functional organisation of the primate visual cortex. In A. Peters & E.G. Jones (Eds.), Cerebral cortex: Volume 3. (pp. 259-329). London: Plenum Press. Van Voorhis, S., & Hillyard, S.A. (1977). Visual evoked potentials and selective attention to points in space. Perception and Psychophysics, 22, 54-62. Wood, C.C. (1982). Application of dipole localisation methods to source identification of human evoked potentials. Annals of the New York Academy of Sciences, 388, 139-155. Wurtz, R.H., Goldberg, M.E., & Robinson, D.L. (1980). Behavioural modulation of visual responses in the monkey: Stimulus selection for attention and movement. Progress in Psychobiology and Physiological Psychology, 9, 43-83.
111
26 (1988) 111-116
LATENCIES OF VISUALLY RESPONSIVE NEURONS IN VARIOUS REGIONS OF THE RHESUS MONKEY BRAIN AND THEIR RELATION TO HUMAN VISUAL RESPONSES * David Lee ROBINSON Laboratory of Sensorimotor
Research, National Eye Institute, Bethesda, MD 20892, U.S.A.
Michael D. RUGG MRC Cognitive Neuroscience Research Group, University of St Andrews, Fife KY16 9JU, U.K.
St Andrews,
The temporal characteristics of visually responsive neurons in a variety of areas of the monkey brain are presented. These data allow a comparison to be made between the latencies of components of the human visual ERP, and the onset latencies of neurons in regions which are candidate sources of these ERP phenomena.
1. Introduction An important aspect of research using human event-related potentials (ERPs) is the identification of the brain structures responsible for the generation and modulation of these scalp-recorded waveforms. Because of the difficulties inherent in inferring the cerebral origins of an ERP effect from its scalp distribution alone (e.g., Wood, 1982), it is desirable also to employ other physiological criteria when these are available. In this regard, consideration of relevant single neuron data from sub-human primates might sometimes help to narrow down the range of possible generators of a given ERP effect. This kind of reasoning has been employed, for example, by Hillyard, Munte and Neville (1985) in their analysis of ERPs in relation to visual-spatial attention. They argued that the sensitivity of the Pl component of the visual ERP to spatial attention was unlikely to reflect activity in areas 17 or 18 of the visual cortex, because single unit studies in monkeys had failed to find neurons in these areas sensitive to spatial attention. The good temporal resolution of scalp-recorded ERPs means that it is possible to compare ERP latencies with those found for changes in the firing * Reprint requests may be directed to either author. during the preparation of this paper.
0301-0511/88/$3.50
We are grateful
0 1988, Elsevier Science Publishers
to Dr V.H. Perry for advice
B.V. (North-Holland)
112
D.L. Robinson and M.D. Rugg / Onset latencies of visual responses
rates of single neurons in the brains of experimental animals. Such comparisons could provide a useful source of information about the possible cerebral origins of ERP components and their modulation, if it is assumed that the neural events generating scalp-recorded potentials are closely allied in time with changes in the activity of single neurons. To take an extreme, hypothetical example, it seems implausible to postulate that an ERP deflection with an onset of 300 ms directly reflects activity in a structure in which single neurons showed enhanced activity within 50 ms post-stimulus. Similarly, it would also seem unlikely that a brain area in which cells do not become active until 100 ms generates an ERP effect with an onset latency of 50 ms. The purpose of the present paper is to provide some information on the timing of visually-responsive neurons in various regions of the monkey brain, thereby allowing ERP researchers to compare their own data with those from relevant animal studies more easily than at present. The brain regions discussed include some which are thought to play a role in visual attention (pulvinar, posterior parietal cortex, area V4 and peri-frontal cortex), form vision (area 17, area 18, area V4 and inferotemporal cortex), and visually-guided eye-movements (superior colliculus and frontal eye fields), and we hope that these data will be of particular benefit to ERP researchers in these and related fields of research. Comparable data may also exist for the auditory and somatosensory systems.
2. Applicability of the data Except for values for the superior colliculus, the data in the present paper come from studies of awake rhesus monkeys. Since these animals are conscious and actively participating in many of the experimental tasks, it is likely that their behavioural states and neural processing would be comparable to human subjects of similar ERP experiments. Many studies have demonstrated that the visual and oculomotor capacities of the two species are remarkably similar (Bough, 1970; Carpenter, 1977; Cavonious & Robbins, 1973; DeValois, Morgan, Polson, Mead, & Hull, 1974; DeValois, Morgan, & Snodderly, 1974; Sarmiento, 1975). Therefore, although direct evidence is lacking, it is reasonable to suppose that the anatomy and function of the human and rhesus monkey visual systems are very similar (Cowey, 1982; Van Essen, 1985). Moreover, although the visual pathways are somewhat longer in humans than monkeys, the effects of this on relative conduction times in the two species is likely to be negligible given the limits of accuracy to which latency measurements can be made. Accordingly, we are assuming that the values derived from the monkey can be used as estimates for the human brain without adjustment.
D.L. Robinson and M.D. Rugg / Onset latencies of visual responses
113
3. The data The data are shown in table 1, and summarised in fig. 1. They consist mainly of the mean onset latencies of visually-responsive neurons in various regions of the brains of conscious monkeys. The onset latencies for individual cells were determined at the point of significant increment of a histogram based on several stimulus presentations. Where possible, the standard deviation and range of the onset latencies of the neurons sampled in a particular region are also presented. Since conduction times can differ for various parts of the visual field, we have also indicated whether the evoking stimuli were presented at fovea1 or extra-foveal locations. Several of the brain areas have been tested during various types of active visual behaviour, and we have noted
Table 1 Onset latencies (ms) of visually-responsive neurons in various areas of the rhesus monkey brain Area
Mean
Sub-cortex Superior Colliculus Pulvinar: Inferior Map Lateral Map Dorsomedial
64 84
Cortex Area 17 Area 18 V4 complex
53 c.d 67 c*d 78 a,c.d
44
66
b.c.d
b,c.d
a b ’ d ’
Range
Reference
_
34-60
Moors and Vendrick (1979)
16 20 48
b.c.d a.c.d
18 _
31 _
58
125 d,e
_ _
_
21 26
80 c.d Middle temporal area Inferotemporal area Superior temporal sulcus Posterior parietal (area 7) Frontal eye-fields (area 8) Peri-frontal cortex (area 46)
SD
70-220 a*c,d (60% < 120)
Petersen et al. (1985) Petersen et al. (1985) Petersen et al. (1985)
Maunsell (pew comm., fall 1987) Maunsell (pers. comm., fall 1987) Both and Fischer (1983) Maunsell (pers. comm., fall 1987) Maunsell (pers. comm., fall 1987) Richmond et al. 1983)
20
Perett et al. (1982)
90 a.c.d 87 b.c.d
31 35
Petersen et al. (1985) Goldberg and Bushnell (1981)
91
16
Both and Goldberg (1987)
a.c.d
Attentionally responsive. Eye-movement modulation. Non-fovea1 stimuli. Fovea1 stimuli. Neurons responsive to face stimuli.
114
D.L. Robinson and M.D. Rugg / Onsst latencies of visual responses POSTERIOR PARIETAL CORTEX (AREA 7) 90 MSEC
FRONTAL EYE FIELDS (AREA 81.
PERIPRINCIPAL CORT (AREA 48) -9l MSEi’
RIATE CORTEX (AREA 17)
PULVINAR’
IDDLE TEMPORAL CORTEX
PI 66 MSEC
58 MSEC
/ INFERIOR TEMPORAL CORTEX
coLLlcuws 44 MSEC
Fig. 1. Schematic view of the lateral surface of the rhesus monkey brain. Each line indicates the location on the brain of a visual area for which a latency has been determined. The brain is drawn as if part of the temporal lobe has been removed to expose the superior colliculus. The diagonally striped region on the temporal lobe represents the general region of the pulvinar nuclei.
whether neurons in each area responded in an attentionally selective fashion, that is whether any enhancement in their firing rates was dependent upon the evoking stimulus being presented within the focus of attention and whether the enhancement was independent of motor responses (Wurtz, Goldberg, & Robinson, 1980) I. Other areas are noted which contain cells selectively enhanced prior to visually-guided saccadic eye-movements.
4. Discussion
A number of points should be made about these data. Firstly, the absolute values should be treated with caution, as changes in such variables as stimulus brightness and retinal eccentricity alter the efficiency of visual processing and would be expected, therefore, to give rise to variations in neuronal onset latencies (Richmond, Optican, Podell, 8z Spitzer, 1987). This should not affect the relative onset latencies of different regions. Secondly, the values represent the beginning of activity and not the time of the most intense response. It is * With the exception of Richmond, Wurtz, and Sato (1983), all the studies noted in table 1 report attentionally selective neurons investigated with visual-spatial attention. Richmond et al. (1983) studied selectivity to different visual patterns presented at the same spatial locus.
D.L. Robinson and M.D. Rugg / Onset latencies of visual responses
115
possible that some stimuli or visual areas have gradual increases in firing whereas others may be more abrupt. Such differences might be expected to be reflected in human ERP onset latencies. Thirdly, changes in stimulus pattern can alter the qualitative nature of the response of an individual neuron. For example, one pattern can evoke a transient burst of activity whereas another visual pattern can elicit inhibition (fig. 9, Richmond et al., 1987). Fourthly, the data allow reasonably firm estimates about the shortest likely onset latency of an ERP effect that is to be attributed to a particular brain region. They do not, however, constrain estimates about the maximum acceptable latency to the same extent. Finally, single neurons vary in the duration of their response to visual stimuli. For some cortical cells there can be a sustained discharge for the duration of a stimulus presentation. For others, there can be a varied pattern of activity for the duration of the stimulus. For yet other cells there is only a transient burst at the onset and/or termination of an image (Richmond et al., 1987). Some cells alter these temporal response patterns with changes in the visual stimulus. In addition, some cortical neurons have sustained discharges which long outlast the brief stimulus which evokes them (Bruce & Goldberg, 1985, fig. 18). It is generally assumed that multiple visual areas subserve different visual functions in the realms of perception and visual behaviour (Van Essen, 1985). Consistent with this hypothesis is the observation that certain types of active behaviour can augment the responsiveness of cells in certain areas. Since in most areas the enhancement is almost simultaneous with the “on response”, this might be expected to increase the amplitude of an ERP effect but not its latency. In area V4 the attentional effects arise about 30 ms after the “on response” (Moran, 1985) and could well change the waveshape of the ERP. It is often assumed that ERPs to visual stimuli recorded at anterior sites are likely to reflect non-specific activity (e.g., NXatanen & Michie, 1979; Van Voorhis & Hillyard, 1977). However, the onset latencies of neurons in areas of frontal cortex implicated in visual processing are comparable with those in several posterior visual areas (e.g., frontal eye fields 87 ms; inferior parietal cortex 90 ms). Since the neural activity in these frontal regions may contribute to scalp-recorded ERPs, the anterior/posterior distribution of a visual ERP component may not be indicative of whether or not it reflects .brain activity specific to the visual modality.
References Both, R. & Fischer, B. (1983). Saccadic reaction times and activation of the prelunate cortex: Parallel observations in trained rhesus monkeys. Experimental Brain Research, 50, 201-210.
116
D. L. Robinson and M.D. Rugg / Onset latencies of visual responses
Both, R., L Goldberg, M.E. (1987). Saccade-related modulation of visual activity in monkey pre-frontal cortex. Investigative Ophthalmology and Visual Science, 28, 124. Bough, E.W. (1970). Stereoscopic vision in the macaque monkey: a behavioural demonstration. Nature, 225, 42-44. Bruce, C.J., & Goldberg, M.E. (1985). Primate frontal eye fields: I. Single neurons discharging before saccades. Journal of Neurophysiology, 53, 603-635. Carpenter, R.H.S. (1977). Movements of the eyes. London: Pion. Cavonious, CR., & Robbins, D.O. (1973). Relationships between luminance and visual acuity in the rhesus monkey. Journal of Physiology (London), 232, 239-246. Cowey, A. (1982). Sensory and non-sensory visual disorders in man and monkey. Philosophical Transactions of the Royal Sociev of London, B 298, 3-13. DeValois, R.L., Morgan, H.C., Polson, M.C., Mead, W.R., & Hull, E.M. (1974). Psychophysical studies of monkey vision: I. Macaque luminosity and color vision tests. Vision Research, 14, 53-67. DeValois, R.L., Morgan, H., & Snodderly, D.M. (1974). Psychophysical studies of monkey vision: III. Spatial luminance contrast sensitivity tests of macaque and human observers. Vision Research, 14, 75-81. Goldberg, M.E., & Bushnell, M.C. (1981). Behavioural enhancement of visual responses in monkey cerebral cortex: II. Modulation in frontal eye fields specifically related to saccades. Journal of Neurophysiology, 46, 773-787. Hillyard, S.A., Munte, T.F., & Neville, H.J. (1985). Visual-spatial attention, orienting and brain physiology. In M.I. Posner & O.S.M. Marin (Eds.), Attention andperformance XI (pp. 63-84). London: Lawrence Erlbaum. Moors, J., & Vendrick, A.J.H. (1979). Responses of single units in the monkey superior colliculus to stationary flashing stimuli. Experimental Brain Research, 35, 333-347. Moran, J.C. (1985). Selective attention gates the processing of visual information in primate extrastriate cortex. Unpublished PhD Thesis, Univeristy of Oregon. Nllt%nen, R., & Michie, P.T. (1979). Early selective-attention effects on the evoked potential: A critical review and reinterpretation. Biological Psychology, 8, 81-136. Perrett, D.I., Rolls, E.T., 65 Caan, W. @982). Visual neurones responsive to faces in the monkey temporal cortex. Experimental Brain Research, 47, 329-342. Petersen, S.E., Robinson, D.L., & Keys, W. (1985). Pulvinar nuclei of the behaving rhesus monkey: Visual responses and their modulation. Journal of Neurophysiology, 54, 867-886. Richmond, B.J., Optican, L.M., Podell, M., & Spitzer, H. (1987). Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex: I. Response characteristics. Journal of Neurophysiology, 57, 132-146. Richmond, B.J., Wurtz, R.H., & Sato, T. (1983). Visual responses of inferior temporal neurons in awake rhesus monkey. Journal of Neurophysiology, 50, 1415-1432. Sarmiento, R.F. (1975). The stereoacuity of macaque monkey. Vision Research, 15, 493-498. Van Essen, D.C. (1985). Functional organisation of the primate visual cortex. In A. Peters & E.G. Jones (Eds.), Cerebral cortex: Volume 3. (pp. 259-329). London: Plenum Press. Van Voorhis, S., & Hillyard, S.A. (1977). Visual evoked potentials and selective attention to points in space. Perception and Psychophysics, 22, 54-62. Wood, C.C. (1982). Application of dipole localisation methods to source identification of human evoked potentials. Annals of the New York Academy of Sciences, 388, 139-155. Wurtz, R.H., Goldberg, M.E., & Robinson, D.L. (1980). Behavioural modulation of visual responses in the monkey: Stimulus selection for attention and movement. Progress in Psychobiology and Physiological Psychology, 9, 43-83.