- Email: [email protected]
Putting things in context
414
News & Comment
TRENDS in Cognitive Sciences Vol.5 No.10 October 2001
Journal Club
Unmasking the neural correlates of conscious perception Which brain areas are involved in consciousness? One way to assess this issue is to investigate brain activity to consciously and unconsciously perceived words, using a phenomenon called ‘masking’. When a word is presented briefly and is immediately preceded or followed by other stimuli (‘masked’), it is often not detected, but is still processed to some degree, as has been shown by behavioral studies. It is therefore interesting for the question of consciousness to see which brain areas are activated by such unconsciously perceived words, and in what sense the activation differs from that in conscious perception. ‘...activation in the ventral visual stream is not sufficient to lead to conscious perception’ Dehaene et al. recorded brain activity using fMRI and ERP while masked and unmasked words were visually presented to the subjects1. From their behavior it was clear that the subjects did not detect the masked words; however, the fMRI showed activation to masked words in the left fusiform gyrus (part of the ventral visual stream) and left precentral sulcus. These areas were among those active for consciously perceived words, although the activation level was reduced for the masked words. Comparable effects were seen in the
ERP data: both consciously and unconsciously perceived words elicited an early positive and an early negative waveform, but the effects were reduced for the unconsciously perceived words. In order to see whether the masked words were actually processed, a second fMRI experiment looked at the effect of a masked word on the processing of a subsequent word. Brain activity is generally reduced to a repeated word. Therefore, if reduced activation were found when a word is preceded by the same masked word, it can be inferred that the masked word is processed to some level. Deheane et al. therefore investigated brain activity to consciously perceived words that were preceded by a masked word. The two words were either the same or two unrelated words. Furthermore, the two words were either printed in the same or a different letter case. When the words were the same, activity to the consciously perceived word was reduced in the left fusiform and left precental gyrus – the same brain areas that were activated by the masked word in the first experiment. Interestingly, this was independent of whether the masked word was presented in a same or a different case, suggesting that the masked word had been processed to a level beyond its physical form. These results thus show that activation in the ventral visual stream is not sufficient
to lead to conscious perception, in contrast to the claims of some other researchers. However, as Dehaene et al. point out, it might be that the level of activation of these areas, or the correlation of activity between visual and distant frontal areas is crucial for conscious perception. In the present study, this correlation was significant for the consciously perceived words, but not for masked words. This suggests that conscious perception involves not so much the activation of specific areas, but the functional connectivity between areas, with frontal regions influencing areas involved in lower-level perception. This is corroborated by data from neglect patients – when these patients report having seen the stimuli in their neglected field, an increased correlation is seen between the activity in ventro-occipital and frontal areas. The present results are therefore very encouraging. Further research is needed to determine whether the correlation in activity between frontal and occipital areas actually causes conscious perception, and is not merely a consequence of it. 1 Deheane, S. et al. (2001) Cerebral mechanisms of word masking and unconscious repetition priming. Nat. Neurosci. 4, 752–758
Edith Kaan [email protected]
Putting things in context Context-sensitivity has been studied in paradigms that are many and various. But do these paradigms reflect any common underlying processes? This issue can be studied by looking for basic physiological mechanisms that could implement various forms of context-sensitivity, and by studying the consequences of their malfunction. Companion papers by Javitt et al.1 and Umbricht et al.2 use this strategy to make major advances towards solving these problems. In doing so they could also lay foundations for a better understanding of some common psychiatric disorders. Context-sensitivity was studied concurrently in post-attentive visual processing and in pre-attentive auditory http://tics.trends.com
processing, in both healthy subjects (in Umbricht et al.) and schizophrenic patients (Javitt et al.). Letters were presented at a rate of 1/s on a computer monitor and subjects were asked to press a button whenever they saw an X, but only if it followed an A (the ‘AX-Continuous Performance Task’ or AX-CPT). Each letter thus formed a context that modulated the response to the next letter. Irrelevant auditory tones were also presented while subjects performed the AXCPT. Most were of a standard pitch and duration, but some deviated in either pitch or duration. Event-related potentials (ERP) were recorded by an array of 36 scalp electrodes. Such recordings usually show
that deviant tones produce larger negative potentials in auditory sensory cortex than standards. This is called mismatch negativity (MMN). Prior tones thus form a context that automatically reduces cortical sensory responses to standards and increases responses to deviants. ‘...some of the cognitive deficits that are associated with schizophrenia can be produced within minutes in healthy volunteers...’ Many human and animal studies provide evidence that contextual modulation involves NMDA-receptors for glutamate, which is the major excitatory
1364-6613/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
neurotransmitter. In their paper, Umbricht et al. examined this possibility by giving healthy volunteers sub-anaesthetic doses of ketamine, which impairs NMDA function. Their placebo-controlled study showed that ketamine caused more errors to BX sequences than to AY sequences in the AX-CPT; that is, letters other than A failed to inhibit the well-rehearsed button-press response to Xs. This shows that ketamine produces a selective deficit of the form of context-sensitivity involved in the AX-CPT. Two different inter-stimulus intervals were used, but the effects of this variable did not interact with drug treatment, showing that the ketamine effect was not the result of more rapid forgetting. ERP measures showed that, as predicted, ketamine also decreased the amplitude of the MMN , but did not affect the context-independent components of the ERP response. Thus, ketamine also produced a selective deficit in the form of context-sensitivity underlying MMN. Javitt et al. used the same combined
TRENDS in Cognitive Sciences Vol.5 No.10 October 2001
AX-CPT and MMN paradigm with schizophrenia patients, because there is a rapidly growing body of evidence suggesting that they have impairments in both context-sensitivity and NMDAmediated neurotransmission. Even though they were not given ketamine, essentially the same results were obtained with the schizophrenic patients as in the healthy subjects who had been given the drug. These findings have important implications. A single pharmacological treatment produced selective impairments of context-sensitivity in both post-attentive visual processing and pre-attentive auditory processing. The results indicate that different forms of context-sensitivity are implemented by common physiological mechanisms that include NMDA-receptors, and they suggest that both these mechanisms and the functions that they could provide are impaired in schizophrenia. Furthermore, some of the cognitive deficits that are associated with schizophrenia can be
415
produced within minutes in healthy volunteers by a temporary and reversible disturbance of neurochemistry. In both the pre- and the post-attentive tests, the relevant contextual information in these studies was provided by preceding stimuli. There are good reasons to suppose that concurrent stimuli can also act as a context, however, so one important task for the future is to study both pre- and post-attentive effects of concurrent context using the general approach pioneered by these researchers. 1 Javitt, D.C. et al. (2000) Deficits in auditory and visual context-dependent processing in schizophrenia. Arch. Gen. Psychiatry 57, 1131–1137 2 Umbricht, D.U. et al. (2000) Ketamine induced deficits in auditory and visual context-dependent processing in healthy volunteers. Arch. Gen. Psychiatry 57, 1139–1147
Bill Phillips [email protected]
Always on my mind: object permanence Object permanence, the ability to understand that objects continue to exist even when they are no longer visible, has been widely studied from both perceptual and cognitive perspectives. One of the most important findings is that the gradual occlusion of an object represents the most effective visual cue leading to object permanence. However, the neural mechanisms underlying this process have, so far, received little attention. A new paper by Baker et al. helps to rectify this state of affairs1. They have identified a neuronal population in the anterior superior temporal sulcus (STSa) that is selectively activated by an object as it gradually disappears from view behind an occluding screen. The STSa is known to be associated with responses to biologically relevant stimuli, such as faces, hands and bodies, and their motion. This area was therefore selected for Baker et al.’s experiment, in which single neurons were isolated in two rhesus macaques. The responses of these neurons were recorded as the experimenter walked around the testing room, went out of view behind occluding screens, and came back into view again after a period of occlusion that lasted between 3 and 20 seconds. Some of these cells were also tested with a number http://tics.trends.com
of different non-biological objects (such as an upright television stand) in order to examine the form selectivity of these cells. Finally, a small number of cells were tested using a large-aperture liquid crystal shutter in order to compare the effect of sudden versus gradual occlusion of the object. ‘As the STSa cells were found to be most active when the object was completely hidden, they could contribute to the perceptual capacity for object permanence’ Of the 274 cells shown to be responsive to visual stumuli in the STSa, 33 (12%) showed increasing activation as the object was gradually hidden from view, and reached maximum activation during the period when the object was hidden altogether. Of the 15 cells tested for form selectivity, 10 (67%) showed a response: 9 of the 10 responded more during the occlusion of the experimenter’s body, but the remaining cell was more responsive to the other objects. Positional effects were also noted, with 80% (24/30) of cells showing differential activity depending on whether occlusion occurred on the right or left side of the testing room. In some cells, this positional effect was also dependent on the distance of testing from
the animal. These positional effects were not linked to the eye position of the monkeys, indicating that fixation on the occluding screen not responsible for the cell responses to hidden stimuli. For 4 of the 5 cells tested with the shutter, there was no response to the sudden disappearance of the experimenter, suggesting that the manner in which the object was occluded was critical in activating the cells. As the STSa cells were found to be most active when the object was completely hidden, the authors suggest that they contribute to the perceptual capacity for object permanence and might be important in maintaining awareness of predators and/or conspecifics when they move out of sight. Most interestingly of all, Baker et al. suggest that the sustained response observed in these single cells goes beyond perceptual experience, and might correspond to a more abstract, conceptual representation of objects. 1 Baker, C.I. et al. Neuronal representation of disappearing and hidden objects in temporal cortex of the macaque. Exp. Brain Res. DOI 10.1007/s002210100828
Louise Barrett [email protected]
1364-6613/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
TRENDS in Cognitive Sciences Vol.5 No.10 October 2001
Journal Club
Unmasking the neural correlates of conscious perception Which brain areas are involved in consciousness? One way to assess this issue is to investigate brain activity to consciously and unconsciously perceived words, using a phenomenon called ‘masking’. When a word is presented briefly and is immediately preceded or followed by other stimuli (‘masked’), it is often not detected, but is still processed to some degree, as has been shown by behavioral studies. It is therefore interesting for the question of consciousness to see which brain areas are activated by such unconsciously perceived words, and in what sense the activation differs from that in conscious perception. ‘...activation in the ventral visual stream is not sufficient to lead to conscious perception’ Dehaene et al. recorded brain activity using fMRI and ERP while masked and unmasked words were visually presented to the subjects1. From their behavior it was clear that the subjects did not detect the masked words; however, the fMRI showed activation to masked words in the left fusiform gyrus (part of the ventral visual stream) and left precentral sulcus. These areas were among those active for consciously perceived words, although the activation level was reduced for the masked words. Comparable effects were seen in the
ERP data: both consciously and unconsciously perceived words elicited an early positive and an early negative waveform, but the effects were reduced for the unconsciously perceived words. In order to see whether the masked words were actually processed, a second fMRI experiment looked at the effect of a masked word on the processing of a subsequent word. Brain activity is generally reduced to a repeated word. Therefore, if reduced activation were found when a word is preceded by the same masked word, it can be inferred that the masked word is processed to some level. Deheane et al. therefore investigated brain activity to consciously perceived words that were preceded by a masked word. The two words were either the same or two unrelated words. Furthermore, the two words were either printed in the same or a different letter case. When the words were the same, activity to the consciously perceived word was reduced in the left fusiform and left precental gyrus – the same brain areas that were activated by the masked word in the first experiment. Interestingly, this was independent of whether the masked word was presented in a same or a different case, suggesting that the masked word had been processed to a level beyond its physical form. These results thus show that activation in the ventral visual stream is not sufficient
to lead to conscious perception, in contrast to the claims of some other researchers. However, as Dehaene et al. point out, it might be that the level of activation of these areas, or the correlation of activity between visual and distant frontal areas is crucial for conscious perception. In the present study, this correlation was significant for the consciously perceived words, but not for masked words. This suggests that conscious perception involves not so much the activation of specific areas, but the functional connectivity between areas, with frontal regions influencing areas involved in lower-level perception. This is corroborated by data from neglect patients – when these patients report having seen the stimuli in their neglected field, an increased correlation is seen between the activity in ventro-occipital and frontal areas. The present results are therefore very encouraging. Further research is needed to determine whether the correlation in activity between frontal and occipital areas actually causes conscious perception, and is not merely a consequence of it. 1 Deheane, S. et al. (2001) Cerebral mechanisms of word masking and unconscious repetition priming. Nat. Neurosci. 4, 752–758
Edith Kaan [email protected]
Putting things in context Context-sensitivity has been studied in paradigms that are many and various. But do these paradigms reflect any common underlying processes? This issue can be studied by looking for basic physiological mechanisms that could implement various forms of context-sensitivity, and by studying the consequences of their malfunction. Companion papers by Javitt et al.1 and Umbricht et al.2 use this strategy to make major advances towards solving these problems. In doing so they could also lay foundations for a better understanding of some common psychiatric disorders. Context-sensitivity was studied concurrently in post-attentive visual processing and in pre-attentive auditory http://tics.trends.com
processing, in both healthy subjects (in Umbricht et al.) and schizophrenic patients (Javitt et al.). Letters were presented at a rate of 1/s on a computer monitor and subjects were asked to press a button whenever they saw an X, but only if it followed an A (the ‘AX-Continuous Performance Task’ or AX-CPT). Each letter thus formed a context that modulated the response to the next letter. Irrelevant auditory tones were also presented while subjects performed the AXCPT. Most were of a standard pitch and duration, but some deviated in either pitch or duration. Event-related potentials (ERP) were recorded by an array of 36 scalp electrodes. Such recordings usually show
that deviant tones produce larger negative potentials in auditory sensory cortex than standards. This is called mismatch negativity (MMN). Prior tones thus form a context that automatically reduces cortical sensory responses to standards and increases responses to deviants. ‘...some of the cognitive deficits that are associated with schizophrenia can be produced within minutes in healthy volunteers...’ Many human and animal studies provide evidence that contextual modulation involves NMDA-receptors for glutamate, which is the major excitatory
1364-6613/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.
News & Comment
neurotransmitter. In their paper, Umbricht et al. examined this possibility by giving healthy volunteers sub-anaesthetic doses of ketamine, which impairs NMDA function. Their placebo-controlled study showed that ketamine caused more errors to BX sequences than to AY sequences in the AX-CPT; that is, letters other than A failed to inhibit the well-rehearsed button-press response to Xs. This shows that ketamine produces a selective deficit of the form of context-sensitivity involved in the AX-CPT. Two different inter-stimulus intervals were used, but the effects of this variable did not interact with drug treatment, showing that the ketamine effect was not the result of more rapid forgetting. ERP measures showed that, as predicted, ketamine also decreased the amplitude of the MMN , but did not affect the context-independent components of the ERP response. Thus, ketamine also produced a selective deficit in the form of context-sensitivity underlying MMN. Javitt et al. used the same combined
TRENDS in Cognitive Sciences Vol.5 No.10 October 2001
AX-CPT and MMN paradigm with schizophrenia patients, because there is a rapidly growing body of evidence suggesting that they have impairments in both context-sensitivity and NMDAmediated neurotransmission. Even though they were not given ketamine, essentially the same results were obtained with the schizophrenic patients as in the healthy subjects who had been given the drug. These findings have important implications. A single pharmacological treatment produced selective impairments of context-sensitivity in both post-attentive visual processing and pre-attentive auditory processing. The results indicate that different forms of context-sensitivity are implemented by common physiological mechanisms that include NMDA-receptors, and they suggest that both these mechanisms and the functions that they could provide are impaired in schizophrenia. Furthermore, some of the cognitive deficits that are associated with schizophrenia can be
415
produced within minutes in healthy volunteers by a temporary and reversible disturbance of neurochemistry. In both the pre- and the post-attentive tests, the relevant contextual information in these studies was provided by preceding stimuli. There are good reasons to suppose that concurrent stimuli can also act as a context, however, so one important task for the future is to study both pre- and post-attentive effects of concurrent context using the general approach pioneered by these researchers. 1 Javitt, D.C. et al. (2000) Deficits in auditory and visual context-dependent processing in schizophrenia. Arch. Gen. Psychiatry 57, 1131–1137 2 Umbricht, D.U. et al. (2000) Ketamine induced deficits in auditory and visual context-dependent processing in healthy volunteers. Arch. Gen. Psychiatry 57, 1139–1147
Bill Phillips [email protected]
Always on my mind: object permanence Object permanence, the ability to understand that objects continue to exist even when they are no longer visible, has been widely studied from both perceptual and cognitive perspectives. One of the most important findings is that the gradual occlusion of an object represents the most effective visual cue leading to object permanence. However, the neural mechanisms underlying this process have, so far, received little attention. A new paper by Baker et al. helps to rectify this state of affairs1. They have identified a neuronal population in the anterior superior temporal sulcus (STSa) that is selectively activated by an object as it gradually disappears from view behind an occluding screen. The STSa is known to be associated with responses to biologically relevant stimuli, such as faces, hands and bodies, and their motion. This area was therefore selected for Baker et al.’s experiment, in which single neurons were isolated in two rhesus macaques. The responses of these neurons were recorded as the experimenter walked around the testing room, went out of view behind occluding screens, and came back into view again after a period of occlusion that lasted between 3 and 20 seconds. Some of these cells were also tested with a number http://tics.trends.com
of different non-biological objects (such as an upright television stand) in order to examine the form selectivity of these cells. Finally, a small number of cells were tested using a large-aperture liquid crystal shutter in order to compare the effect of sudden versus gradual occlusion of the object. ‘As the STSa cells were found to be most active when the object was completely hidden, they could contribute to the perceptual capacity for object permanence’ Of the 274 cells shown to be responsive to visual stumuli in the STSa, 33 (12%) showed increasing activation as the object was gradually hidden from view, and reached maximum activation during the period when the object was hidden altogether. Of the 15 cells tested for form selectivity, 10 (67%) showed a response: 9 of the 10 responded more during the occlusion of the experimenter’s body, but the remaining cell was more responsive to the other objects. Positional effects were also noted, with 80% (24/30) of cells showing differential activity depending on whether occlusion occurred on the right or left side of the testing room. In some cells, this positional effect was also dependent on the distance of testing from
the animal. These positional effects were not linked to the eye position of the monkeys, indicating that fixation on the occluding screen not responsible for the cell responses to hidden stimuli. For 4 of the 5 cells tested with the shutter, there was no response to the sudden disappearance of the experimenter, suggesting that the manner in which the object was occluded was critical in activating the cells. As the STSa cells were found to be most active when the object was completely hidden, the authors suggest that they contribute to the perceptual capacity for object permanence and might be important in maintaining awareness of predators and/or conspecifics when they move out of sight. Most interestingly of all, Baker et al. suggest that the sustained response observed in these single cells goes beyond perceptual experience, and might correspond to a more abstract, conceptual representation of objects. 1 Baker, C.I. et al. Neuronal representation of disappearing and hidden objects in temporal cortex of the macaque. Exp. Brain Res. DOI 10.1007/s002210100828
Louise Barrett [email protected]
1364-6613/01/$ – see front matter © 2001 Elsevier Science Ltd. All rights reserved.