Effects of nonconscious perception on motor response

Human Movement Science 21 (2002) 541–561 www.elsevier.com/locate/humov

Effects of nonconscious perception on motor response Kuniyasu Imanaka *, Ichiro Kita, Kunitake Suzuki Department of Kinesiology, Graduate School of Science, Tokyo Metropolitan University, 1-1 Minami-Ohsawa, Hachioji, Tokyo 192-0397, Japan

Abstract The present study reviews the literature on the empirical evidence for the dissociation between perception and action. We first review several key studies on brain-damaged patients, such as those suffering from blindsight and visual/tactile agnosia, and on experimental findings examining pointing movements in normal people in response to a nonconsciously perceived stimulus. We then describe three experiments we conducted using simple reaction time (RT) tasks with backward masking, in which the first (weak) and second (strong) electric stimuli were consecutively presented with a 40-ms interstimulus interval (ISI). First, we compared simple RTs for three stimulus conditions: weak alone, strong alone, and double, i.e., weak plus strong (Experiment 1); then, we manipulated the intensity of the first stimulus from the threshold (T ) to 1:2T and 2T , with the second stimulus at 4T (Experiment 2); finally, we tested three different ISIs (20, 40, and 60 ms) with the stimulus intensities at 1:2T and 4T for the first and second stimuli (Experiment 3). These experiments showed that simple RTs were shorter for the double condition than for the strong-alone condition, indicating that motor processes under the double condition may be triggered by sensory inputs arising from the first stimulus. Our results also showed that the first stimulus was perceived without conscious awareness. These findings suggested that motor processes may be dissociated from conscious perceptual processes and that these two processes may not take place in a series but, rather, in parallel. We discussed the likely mechanisms underlying nonconscious perception and motor response to a nonconsciously perceived stimulus. Ó 2002 Elsevier Science B.V. All rights reserved. PsycINFO classification: 2320; 2330; 2380 Keywords: Nonconscious perception; Simple reaction time; Somatosensory backward masking

*

Corresponding author. E-mail address: [email protected] (K. Imanaka).

0167-9457/02/$ - see front matter Ó 2002 Elsevier Science B.V. All rights reserved. doi:10.1016/S0167-9457(02)00175-6

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1. Introduction A number of neuropsychological studies have reported behavioural evidence for motor responses to stimuli perceived without awareness (i.e., nonconscious perception), demonstrating empirical findings observed in several brain-damaged patients. Some examples are cases of blindsight (Weiskrantz, Warrington, Sanders, & Marshall, 1974), visual-form agnosia (Goodale, Milner, Jakobson, & Carey, 1991), and touch/proprioceptive agnosia (Rossetti, Rode, & Boisson, 1995). These cases of brain-damaged patients have indicated evidence for both nonconscious perception and accurate motor responses (e.g., pointing) to nonconsciously perceived stimuli, thus demonstrating the typical dissociation between perception and action (e.g., Rossetti, 1998). Such dissociation between perception and action has also been shown in several experimental studies (e.g., Aglioti, DeSouza, & Goodale, 1995; Bridgeman, Kirch, & Sperling, 1981; Goodale, Pelisson, & Prablanc, 1986; Taylor & McCloskey, 1990, 1996) examining visual perception and motor response in neurologically normal participants. However, most of these studies using normal participants have dealt with the visual modality alone. Concerning the kinesthetic and/or somatosensory modalities, which are crucial in motor action, only a few studies have attempted to examine the relationship between nonconscious perception and action (e.g., MacIntyre & McComas, 1996; Takai, Imanaka, Kita, & Mori, 2000). In the present study, we first describe neuropsychological evidence for nonconscious perception and action, as in several brain-damaged patients in both visual (Goodale et al., 1991; Weiskrantz et al., 1974) and tactile (Rossetti et al., 1995) sensory modalities. We then review several studies (Aglioti et al., 1995; Bridgeman et al., 1981; Goodale et al., 1986; Taylor & McCloskey, 1996) using normal participants to examine the dissociation between visual perception and action. Finally, we report our empirical data of nonconscious perception and action, which were examined using a somatosensory reaction time (RT) task with a backward-masking paradigm.

2. Nonconscious perception and action in brain-damaged patients 2.1. Blindsight A typical example of nonconscious perception is blindsight. Weiskrantz et al. (1974) examined a brain-damaged patient, D.B., who had visual deficits in the left visual field due to brain lesions in the right occipital lobe. When a light spot was presented for 3 s in the patientÕs left visual field, he accurately pointed to the spot with his finger without any eye movement. Patient D.B. also successfully discriminated between horizontal and vertical lines and between pairs of letters, such as ‘‘X’’ and ‘‘O’’, presented for an unlimited length of time; the stimuli were all presented in his damaged left visual field, and the patient kept his eyes fixed on a fixation point. These findings suggest that patient D.B. could accurately perform some motor and perceptual responses to a given stimulus even though he was blind to the stimulus. Weiskrantz et al. explained that blindsight may be mediated by the neural pathway

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from the retina to the posterior parietal cortex via the superior colliculus (see also Rossetti, 1998), bypassing the visual pathway projecting from the lateral geniculate nucleus (LGN) to the primary visual cortex (where the brain lesions existed). The pathway involving the superior colliculus, the so-called secondary or extra-geniculate visual system, is primarily concerned with the detection of salient visual events, such as moving objects rather than stationary ones, orientation to visual events in space, and saccadic eye movements (Wurtz & Optican, 1994). The functions of this visual system are quite different from those of the geniculate visual system, which involves both the ventral (responsible for visual perception of colour and shape of an object) and dorsal (responsible for visuospatial/motor functions) visual pathways (see Goodale, 1998). Given the brain lesions of D.B. in the right occipital cortex, Weiskrantz et al. proposed the extra-geniculate visual system as a likely cause of the blindsight of patient D.B. 2.2. Visual-form agnosia A case of visual-form agnosia observed in a brain-damaged patient, D.F., has been reported by Goodale et al. (1991). Patient D.F. was able to accurately perform motor action to visual stimuli, such as catching a fly ball. Goodale et al. examined the perceptual and motor performance of D.F. in a task in which a slot (12:5
3:8 cm) was presented in front of her in various directions so that she could insert her hand into the slot. When asked to describe the direction of the slot verbally, patient D.F. gave incorrect answers as a result of her visual-form agnosia. Nevertheless, when she was asked to insert her own hand or a card into the slot (i.e., simulating the placement of mail in a postal slot), she successfully performed the action as if she could see the slot well. Goodale et al. explained that the locus of D.F.Õs deficit was at a part of the ventral visual pathway, which is assumed to be responsible for the perception of form and colour, and that this led to her incorrect verbal responses. The authors explained that D.F.Õs accurate actions were due to the fact that her dorsal visual pathway, which was credited with the perception and response to spatial information, was intact. Patient D.F. thus showed a behavioural dissociation between perception and action, although the explanation was quite different from that for the blindsight in patient D.B. described in the previous section. 2.3. Tactile/somatosensory agnosia A case of dissociation involving perception and action in a tactile or somatosensory modality was shown by Rossetti et al. (1995). They used a tactile stimulation task to test a patient, J.A., who had a brain lesion of the left ventrolateral (VL) and ventroposterior lateral (VPL) nuclei of the thalamus resulting in total sensory loss on the right side of the body. When J.A. was blindfolded and stimulated by a stylus on the fingertips, palm, and wrist of the right hand, he was unable to identify the stimulated locations; on the other hand, when he was asked to point out the location of the stimulus using his left, intact hand, he made relatively accurate responses that could not have been just the result of chance. Furthermore, when

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J.A. was asked to perform a pointing action with his left hand, either with a concurrent verbal report about the stimulated location or by pointing at a picture of the right hand, his motor performance deteriorated. These results indicated that, although J.A. was unaware of the stimulation, he could accurately perform a pointing action with his intact left hand despite the absence of awareness of perception. The interpretation of this phenomenon by Rossetti et al. was that the neural pathways projecting from the skin receptors to the posterior parietal cortex via the medial region of the posterior nuclei (POM) at the thalamus were intact, bypassing the VPL (where the brain lesion existed) and the primary somatosensory cortex. These behavioural phenomena suggest that humans potentially have neural pathways that are irrelevant to the conscious awareness of perceiving a given stimulus when producing a motor response to the stimulus.

3. Dissociation between perception and action in neurologically normal people 3.1. Pointing action to an induced motion The question of whether the dissociation between perception and action occurs in neurologically normal people has often been raised. A number of findings support a positive response to this question. For example, Bridgeman et al. (1981) reported experiments in which an induced motion of a visual target was used, with a random dot pattern as a background. The random dot pattern was repetitively displaced (1.66 Hz) in a horizontal, left and right direction. Participants were asked to visually track a black square at the centre of the random dot pattern, thus performing repetitive saccadic eye movements in the same phase as the background oscillation. During the background oscillation, the visual target was either standing still (thus, the participants perceived an induced motion of the target) or moved in the same phase as the background oscillation (thus, no induced motion occurred, and the target was then perceived as stationary). After about two full cycles of these displacements, both the target and the background pattern disappeared simultaneously. The participants were then asked to point at the target position by operating an unseen pointer at a position directly under the target that had disappeared. When the target was standing still, pointing was performed toward the actual position of the target rather than the perceived position due to the induced motion. When the target was displaced in the same phase as the background oscillation, pointing was biased toward the actual target position as well as toward the centre of oscillation. Bridgeman et al. concluded that pointing generally followed the actual position when the actual position and the perceived, apparent position were dissociated, suggesting that the output of the motor system can be isolated from the cognitive system by eliminating image information during the motor pointing procedure. The finding by Bridgeman et al. showed an example of the dissociation between perception and action in neurologically normal people, although the experimental situation used by Bridgeman et al. seemed to be unusual compared to our daily circumstances because only the target and the background pattern were visible in the dark room.

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3.2. Pointing action for an object moved during a saccadic eye movement Goodale et al. (1986) and Pelisson, Prablanc, Goodale, and Jeannerod (1986) also showed empirical evidence for the dissociation between perception and action in normal people. They conducted an experiment using double-step stimulation. In the experiment, participants fixed their eyes on a light spot, which suddenly moved 30, 40 or 50 cm to the right. The participants were asked to point as quickly as possible when the spot moved. This was a single-step condition. In some other trials, the spot was moved 10% further away from the first sudden shift of the spot or 5% closer in a direction opposite to the first shift. This was the double-step condition. In the double-step condition, the second shift of the spot was executed during a saccadic eye movement taking place toward the light spot moved by the first shift. It is well known that visual information processing is suppressed during saccadic eye movements (Shioiri & Cavanagh, 1989; Volkmann, Schick, & Riggs, 1968). This means that the participants should not be able to see the second shift of the spot. Nevertheless, the participants accurately performed pointing movements in a single smooth motion (i.e., with a bell-shaped velocity profile) without any additional correctional movements, even under the double-step condition. This indicates that the participants successfully corrected their pointing movements smoothly without awareness of seeing the second shift of the spot. This can also be explained in terms of the second visual pathway, that is, the pathway involving the superior colliculus and bypassing both the LGN and the primary visual cortex. 3.3. Effects of size-contrast illusion on perception and action A series of studies by Goodale and colleagues (Aglioti et al., 1995; Danckert, Sharif, Haffenden, Schiff, & Goodale, 2002; Haffenden & Goodale, 1998; Haffenden, Schiff, & Goodale, 2001) on the effect of size-contrast (or Titchener Circles) illusion on perception and action demonstrated another example of dissociation between perception and action. This type of illusion typically occurs when two sets of circle arrays, each consisting of an annulus of circles and a centre circle, are presented side by side: for one array, the annular circles are larger than the centre circle, while, for the other, the annular circles are smaller than the centre circle, with the two centre circles being equivalent in size. When comparing the two centre circles, observers would be under the illusion that the centre circle accompanied by larger annular circles was smaller than the centre circle accompanied by smaller annular circles. Aglioti et al. (1995) conducted an experiment in which participants were asked to either estimate the size of a disk, placed as the centre circle, by adjusting the aperture between their thumb and the index finger (a manual estimation task) or just pick up the disk by the thumb and index finger (a grasping task). The manual estimations of disk size were shown to be biased in the direction of the illusion, while the maximum grip size during the grasping movement was strongly correlated with the physical size of the disk. This suggests that the grip size is calibrated to the true size of the disk, even when the perception of the disk is distorted by visual illusion. This phenomenon was strongly demonstrated, even when visual feedback from both the hand and the disk

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was eliminated during either the grasping or the estimating task (Haffenden & Goodale, 1998) and also even at the early stages of the grasping movement (Danckert et al., 2002). The implication is that both the initial planning and the online control of an object-directed grasping movement are refractory to the effects of illusion. These findings have been interpreted to indicate that the dissociation between vision for perception and vision for action is mediated by the operation of the two separate streams (the dorsal and ventral) of visual processing in the brain (Goodale & Milner, 1992). 3.4. Motor response under visual backward masking Another typical example of the perception–action dissociation can be seen in visual RT studies with a backward-masking paradigm. Backward masking has often been used as a traditional experimental paradigm to examine visual awareness and/or visual subliminal perception (Eriksen & Collins, 1965; Fehrer & Biederman, 1962; Fehrer & Raab, 1962; Schiller & Smith, 1966). In the last decade, the paradigm of backward masking in RT tasks has been applied to examinations of the relationships between motor action and nonconscious perception (Klotz & Neumann, 1999; Neumann & Klotz, 1994; Taylor & McCloskey, 1990, 1996). Taylor and McCloskey (1996) conducted an RT experiment using a metacontrast (a type of backward-masking) paradigm, in which a 5-ms dim LED (test) was presented 50 ms prior to the presentation of four 50-ms bright LEDs (mask) surrounding the test LED. In such a condition, the participants were unaware of the test LED, since conscious perception was suppressed by the mask LEDs. However, when they were asked to respond to the metacontrast stimulus set (i.e., the set of test and mask LEDs) as fast as possible using a motor action, their RTs were shorter than those in conditions under which the mask stimulus alone was presented. These results suggested that the participants responded to the test LED even though they were unaware of it. This finding is generally consistent with other recent studies (e.g., Klotz & Neumann, 1999; Neumann & Klotz, 1994). Suzuki and Imanaka (2001) also examined the dissociation between visual perception and motor response, comparing the response speeds of a verbal report in a discrimination task and the motor response in a simple RT task. In both tasks, a metacontrast stimulus set (test plus mask stimuli) was used. The participants were asked to report verbally whether or not they perceived the first stimulus from the metacontrast stimulus set in the discrimination task; on the other hand, they were asked to respond to the metacontrast stimulus set as fast as possible in the simple RT task. The stimulus onset asynchrony (SOA) between the test and mask stimuli was manipulated from 0 to 120 ms. The RT of the verbal report became shorter as the SOA became longer. This may be because the participants started to see the test stimulus more clearly as the SOA became longer. In contrast, the speed of motor response in the RT task did not change with the SOAs, even at relatively long SOAs in which the participants were clearly aware of the test stimulus. These results suggest that a verbal report (which may be mediated by conscious awareness) and RT (motor response) are characterised by different temporal features under metacontrast

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masking. This finding also provides evidence for the dissociation between conscious perception and action. 3.5. Motor response under tactile/somatosensory backward masking Most studies on dissociation between conscious perception and action using backward masking have been concerned with vision. Motor action should be largely mediated by tactile and somatosensory information as well as vision. Issues with respect to tactile and somatosensory modalities have been examined by a number of studies on perceptual threshold (Johansson & Vallbo, 1979), conscious awareness (Gomes, 1998; Libet, 1965; Libet, Wright, Feinstein, & Pearl, 1979, 1992), and forward/backward masking (Abramsky, Carmon, & Benton, 1971; Craig & Evans, 1995; Kirman, 1984; Laskin & Spencer, 1979; Schmid, 1961). Nevertheless, only a few studies (MacIntyre & McComas, 1996; Takai et al., 2000) have attempted to examine the issues of motor response under nonconscious tactile/somatosensory perception using backward masking. A pioneer study on motor response under tactile/somatosensory backward masking was conducted by MacIntyre and McComas (1996). They examined choice RTs under a typical backward-masking paradigm, in which both weak (barely perceptible) and strong (but not painful) electric stimuli were delivered on the thumb with an 81-ms interstimulus interval (ISI). Participants were asked to respond to the electric stimuli by reaching with their hand to one of two targets, one for the weak stimulus and the other for the strong one. RTs were compared between the backward-masking condition (i.e., weak plus strong stimuli) and the weak- or strong-alone condition. The RTs were shorter for the backward-masking condition than for either the strong-alone or the weak-alone condition. However, the participants were unaware of the presentation of the weak stimulus in the backward-masking condition. This implies that the participants responded to the weak stimulus even though the weak stimulus was not consciously perceived, which provides evidence for the dissociation between perception and action.

4. Our series of simple RT experiments using somatosensory backward masking 4.1. Experiment 1: A modified replication of the MacIntyre and McComas study We (Takai et al., 2000) recently conducted an experiment that was similar to the MacIntyre and McComas (1996) experiment but used a simple RT task. Choice RTs generally involve various stages of information processing, such as the detection and identification of a given stimulus, selection of a response to be performed, and response programming for preparing motor commands sent to the relevant muscles (Schmidt & Lee, 1999). Therefore, the choice RT should be interpreted in terms of all these information-processing stages. In contrast, simple RTs involve primarily the stimulus detection and motor programming stages because there is no need to identify the nature of a given stimulus or for selecting an appropriate response

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(it should be predetermined). Our intention was to focus on the relationships between stimulus detection (with or without awareness) and motor response under backward masking by using a simple RT task. The participants were nine healthy male volunteers, aged 21–38 years. The experimental task was a quick key response (pressing a computer mouse button with the right index finger) to a given electric stimulus or stimulus set under three stimulation conditions, i.e., double, weak, and strong. In the double condition, weak (a little above the sensory threshold) and strong (about four or five times stronger than the threshold) electric stimuli were consecutively presented, with a 40-ms ISI. In the weak and strong conditions, either the weak or strong stimulus alone was used. The electric stimulus used for both the weak and strong stimuli was a rectangular pulse, 0.2 ms in duration and about 5–100 V in amplitude, delivered on the median nerve at the right wrist through a pair of surface electrodes using an electric stimulator (Nihon-Kohden, SEN-3301) with an isolator (Nihon-Kohden, SS-201J). Prior to determining the intensities of both the weak and strong stimuli, the sensory threshold of the participant was estimated by the method of limits. The electric stimuli were consecutively delivered every 2 s onto the participantÕs wrist, with the intensity of the stimulus being changed stepwise by 1 V in either the ascending or the descending order. The ascending and descending series of stimuli were presented three times each in a random order for a total of six series of stimulus presentation. The threshold intensity was measured in each series of stimulus presentation. The mean value of the six threshold intensities was then calculated, and this was used as the representative threshold intensity for the participant. The intensity of the weak stimulus was determined at a minimum intensity at which the participant was able to perceive it when it was presented alone. The resultant intensities of the weak stimulus for the nine participants ranged from 1.2 to 1.5 times stronger than the sensory threshold. The intensity of the strong stimulus was set just below the pain level so that the participants were not able to consciously perceive the weak stimulus under the double condition. This resulted in the strong stimulus ranging from about 4–5 times stronger than the sensory threshold. Each participant performed the simple RT task in two blocks of 30 trials, consisting of 10 trials for each stimulation condition, for a total of 60 trials. The presentation order of the three stimulation conditions was randomised in each trial block, with a short rest between them. The RT patterns of all participants were similar (Fig. 1). The mean RT of the double condition (M ¼ 310 ms, SD ¼ 39:6), measured as the duration from the onset of the strong stimulus to a key response, was significantly shorter (tð8Þ ¼ 7:25, p < 0:001) than that for the strong condition (M ¼ 338 ms, SD ¼ 41:9), the mean RT of the weak condition (M ¼ 418 ms, SD ¼ 69:0) being the longest. These results suggested that the participants may have responded to the first (weak) stimulus under the double condition, thus shortening the RTs. Introspective reports about whether or not the participants discriminated between the double and strong conditions were collected from each participant. The introspective reports indicated that the participants failed to discriminate between the two conditions and, therefore, were not consciously aware of the weak stimulus in the double condition. This showed that the intensities used for the weak and strong stimuli successfully caused

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Reaction Time (ms)

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H.A.

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H.H. K.Ku. K.Ki. H.U.

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Participants Fig. 1. Mean RTs in ms for weak, double, and strong stimulation conditions for each participant. The RTs for the double condition were measured from the onset of the second stimulus. All participants showed similar patterns of RTs for the three conditions, with the weak RTs being the longest and the double ones the shortest among the three stimulation conditions. [Adapted with permission of the Japan Society of Physical Education, Health, and Sport Sciences from Takai et al., 2000].

a masking effect under the double condition. These results suggested that the participants responded to a weak stimulus that was perceptually masked by the second, strong stimulus. This implies that a nonconsciously perceived stimulus may facilitate motor-related information processing, such as response programming, and that conscious perception and action may be dissociated. 4.2. Experiment 2: Effects of varying stimulus intensities We further examined the relationships between RTs and conscious awareness by manipulating the intensity of the weak stimulus (unpublished data). The primary examination in Experiment 2 was focused on whether a simple RT was a function of conscious awareness of perception or a function of stimulus intensity per se, irrespective of conscious awareness. Seven healthy male volunteers, aged 21–38 years, participated in this experiment. Stimulation conditions were the same as those in Experiment 1, that is, weak (weak alone), strong (strong alone), and double (weak plus strong). For the weak stimulus, we used three stimulus intensities: sensory threshold (T ), 1.2 times larger than the threshold (1:2T ), and two times larger than the threshold (2T ). The intensity of the strong stimulus was four times (4T ) larger than the sensory threshold. Each participant performed the task in two blocks of 30 trials (i.e., 60 trials total) at each stimulus intensity, with the three stimulation conditions randomly presented within each block, for a total of 180 trials per participant. After the simple RT task, each participant performed a discrimination task. In the discrimination task, the three stimulation conditions (weak, double, and strong) were also randomly presented, with the weak stimulus being presented at either T , 1:2T or 2T , in the same procedure

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as in the simple RT task. The participant was instructed to guess the type of stimulation condition and report it verbally. Other experimental procedures were the same as those in Experiment 1. Fig. 2A shows the mean RTs under the weak, double, and strong conditions for T , 1:2T , and 2T stimulus intensities, respectively. An ANOVA on the RT data (the RTs for the double condition were measured from the strong stimulus) showed significant main effects for both the stimulation condition (F ð2; 12Þ ¼ 96:7, p < 0:01) and the stimulus intensity (F ð2; 12Þ ¼ 58:0, p < 0:01), the interaction between these two factors also being significant (F ð4; 24Þ ¼ 15:4, p < 0:01). Subsequent multiple comparisons by the Scheffe test showed that the mean RTs for both the 1:2T and 2T intensities under the double condition were significantly shorter than those under the strong condition, whereas the mean RT for the T intensity under the double condition did not significantly differ from that under the strong condition. Fig. 2B shows the results of the discrimination task. The mean proportions of correct judgment for the double condition appeared to be 55%, 57%, and 90% for T , 1:2T , and 2T , respectively. The mean proportion of correct judgment for neither T (tð6Þ ¼ 0:88, p > 0:2) nor 1:2T (tð6Þ ¼ 1:23, p > 0:1) was significantly different from the chance level (i.e., 50%), while that for 2T was significantly higher than the chance level (tð6Þ ¼ 8:82, 450 T 400 1.2T 350 300

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Fig. 2. (A) Mean RTs in ms for weak, double, and strong stimulation conditions for T , 1:2T , and 2T in intensity for the first stimulus. The circle, triangle, and square indicate T , 1:2T , and 2T , respectively. The open symbols indicate the RTs measured from the onset of the first (weak) stimulus, and the filled symbols indicate the RTs from the onset of the second (strong) stimulus. (B) Mean proportions (%) of correct judgment for weak, double, and strong conditions for T , 1:2T , and 2T intensities.

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p < 0:0001). These results suggested that the participants did not consciously perceive either the T or the 1:2T weak stimulus under the double condition. These results indicated that the T stimulus under the double condition was not consciously perceived by the participants and did not facilitate the motor response, while the 2T stimulus was consciously perceived and, thus, facilitated the motor response. In contrast, for the 1:2T stimulus, the participants were unaware of the 1:2T stimulus; nevertheless, this stimulus facilitated the response speed, resulting in the RTs being significantly shorter than those for the strong condition. This means that motor response and conscious awareness can be dissociated from each other and that, even when a given stimulus is not consciously perceived (such as for the 1:2T stimulus), a motor response can be facilitated. This may depend on the intensity of the first stimulus. If the first stimulus is relatively strong, such as 1:2T and 2T , a motor response can be facilitated (thus, resulting in a short RT) irrespective of the conscious awareness for the first stimulus. Conversely, if the first stimulus is very weak, such as around the threshold, a motor response may not be facilitated. 4.3. Experiment 3: effects of varying the intervals between the first and second stimuli We further manipulated ISIs between the first and second stimuli to be 20, 40 or 60 ms in Experiment 3 (unpublished data). Seven male volunteers, aged 21–38 years, participated in this experiment. The intensity was determined at 1:2T and 4T for the weak and strong stimuli, respectively. It was under this condition that both the effects of backward masking (57% correct judgment) and response facilitation (shortened RTs) were observed in Experiment 2. Other experimental conditions were the same as those in Experiment 2. The primary examination in Experiment 3 was focused on whether the simple RT was a function of ISIs between the first and second stimuli. If the first stimulus triggers subsequent motor processes, then simple RTs should become shorter as the ISI between the first and second stimuli becomes longer (i.e., the first stimulus is presented earlier). Fig. 3A shows simple RTs for the weak and strong conditions as well as for the 20-, 40-, and 60-ms ISIs between the stimuli under the double condition. Paired ttests (with a level set at 0:05=8 ¼ 0:00625 by Bonferroni correction) showed that the RTs measured from the second stimulus (filled squares in Fig. 3A) for both the 60- and 40-ms ISIs were significantly shorter than that for the strong condition (tð6Þ ¼ 3:78, p < 0:005, for 60 ms; tð6Þ ¼ 3:15, p ¼ 0:009, for 40 ms, although nearly significant), while the RT for the 20-ms ISI was not significantly shorter than that for the strong condition (tð6Þ ¼ 1:52, p > 0:08). The difference in the RTs was not significant either between 60- and 40-ms ISIs (tð6Þ ¼ 1:18, p > 0:1) or between 40and 20-ms ISIs (tð6Þ ¼ 1:54, p > 0:08). In contrast, paired t-tests performed on the RTs measured from the first stimulus (open squares in Fig. 3A) showed significant differences both between the weak and the 60-ms ISI conditions (tð6Þ ¼ 5:54, p < 0:0008) and between the 60- and 40-ms ISIs (tð6Þ ¼ 6:69, p < 0:0003) but not between the 40- and 20-ms ISIs (tð6Þ ¼ 0:67, p > 0:2). These results generally indicated that the motor response was facilitated under the double condition, but this was evident for ISIs longer than 40 ms. However, the first

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(B) Fig. 3. (A) Mean RTs in ms for weak, strong, and three double conditions at 20-, 40-, and 60-ms ISIs. The open squares indicate the RTs measured from the onset of the first (weak) stimulus, and the filled ones indicate the RTs from the second (strong) stimulus. (B) Mean proportions (%) of correct judgment for weak, strong, and three double conditions at 20-, 40-, and 60-ms ISIs. The vertical bars attached to each square symbol indicate standard errors of the mean.

stimulus did not facilitate the motor response more for the 60-ms than for the 40-ms ISI, suggesting that the facilitation, or triggering, effect by the first stimulus may not occur more efficiently even when the first stimulus is presented earlier. Instead, when the second stimulus was presented earlier or closer to the first stimulus (i.e., for the 40-ms ISI compared to the 60-ms; see open squares in Fig. 3A), the motor response was significantly more facilitated by the second stimulus. It is therefore suggested that the facilitation of the motor response may first be triggered by the first stimulus and then further activated by the second stimulus. Fig. 3B shows the results of the discrimination task, indicating the mean proportions of correct judgment for the five stimulation conditions. The mean proportion of correct judgment for the weak condition was perfect (100%), and that for the strong condition (80%) differed significantly from the chance level, 50% (tð6Þ ¼ 4:96, p < 0:0013). For the three ISI conditions, the proportions of correct judgment for 20-ms ISI (53%) did not significantly differ from 50% (tð6Þ ¼ 0:32, p > 0:3), suggesting that the participants did not consciously perceive the first stim-

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ulus at all. Neither for the 40-ms (70%) nor for 60-ms (68%) ISI condition did the proportion of correct judgment significantly differ from 50% (tð6Þ ¼ 2:65, p ¼ 0:019, for 40 ms; tð6Þ ¼ 1:76, p ¼ 0:064, for 60 ms), although these were marginal (with a set at 0:05=4 ¼ 0:0125 by Bonferroni correction). The participants did not seem to discriminate clearly the double condition with either the 40- or the 60-ms ISI from the strong condition. In addition, these results showed no clear (e.g., linear) relationship between the RTs and discrimination performances. 4.4. Implications of our findings Our series of experiments showed that a stimulus perceived without conscious awareness can facilitate a motor response. It has traditionally been thought that a motor response to a given stimulus is generally performed after the completion of perceptual processes (such as stimulus detection and/or identification), as suggested by Schmidt and Lee (1999). However, our findings suggest that information processing for a motor response may take place without conscious awareness of stimulus detection. Motor responses can thus be triggered directly by sensory inputs without conscious awareness, although the underlying neural mechanisms are far from clear. The following sections describe some plausible mechanisms underlying nonconscious perception and its role in facilitating, or triggering, information processing that is relevant to producing a motor response.

5. Mechanisms underlying nonconscious perception and facilitated motor responses under backward masking 5.1. Perceptual processes under backward masking 5.1.1. Perceptual nature of a weak stimulus In the backward-masking paradigm, the stimulus intensity of the first stimulus must be very weak, such as at a threshold or just above it (MacIntyre & McComas, 1996; Takai et al., 2000; Taylor & McCloskey, 1990, 1996). As described by PieronÕs law (see Mansfield, 1973), a simple RT is a function of the intensity of a given stimulus. This is generally suggested for visual, auditory, and tactile/somatosensory modalities (Raab, Fehrer, & Hershenson, 1961; Ulrich, Rinkernauer, & Miller, 1998). Burbeck (1985) and Burbeck and Luce (1982) showed relatively long simple RTs, in a range of about 500–1000 ms, for extremely weak auditory stimuli. Our results also showed long simple RTs for the weak condition (see Figs. 1–3). This may be because the first stimulus we used was only above the threshold and it was therefore difficult to detect the first stimulus in a short time. 5.1.2. Detection of the first stimulus and conscious awareness Under the backward-masking paradigm, where the first (weak) stimulus is followed by the second (strong) stimulus, conscious awareness of sensing the first stimulus is often masked by the second stimulus. However, this does not mean that the

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first stimulus under backward masking is not detected by the brain. Libet, Alberts, Wright, and Feinstein (1967) examined the somatosensory evoked potentials (SEPs) that were evoked by presenting 500 times an electric subliminal stimulus whose intensity was 60–85% lower than the sensory threshold. Libet et al. reported that a slight 25-ms SEP component appeared. The 25-ms component of SEP is indicative of sensory inputs reaching the primary somatosensory cortex. It is therefore suggested that subliminal sensory inputs can reach the cerebral cortex even when there is no conscious awareness. Accordingly, the first stimulus we used in our experiments (at least stronger than the threshold) should reach the cerebral cortex even when the stimulus cannot be consciously perceived. Libet and his colleagues (Libet, 1965; Libet et al., 1979, 1992) also conducted a series of experiments in which a combination of both peripheral (skin of the distal part of a limb, with a near-threshold intensity) and central (somatosensory cortex and/or thalamus) electric stimulation was used with various time intervals between the peripheral and central stimulation. Their results showed that retroactive (i.e., backward) masking of the awareness of the peripheral stimulation arose when the onset of the central stimulus was delayed as long as 200–500 ms after the peripheral stimulation. This was typically observed when the central stimulation was applied on a relatively wide area (using a 1-cm disk electrode) of the somatosensory cortex, while, when the area of the central stimulation was relatively small (using a 1-mm disk electrode), retroactive enhancement, rather than masking, of the sensation occurred due to the peripheral stimulation. On the basis of these findings, Libet et al. (1992) suggested that conscious perception of a weak somatosensory stimulus may take as long as 500 ms to arise. More recently, Gomes (1998) suggested that it may take at least 230 ms, although this issue is still in controversy (Gomes, 2002; Libet, 2000). All these reports indicate that extremely weak, or even under-threshold, somatosensory stimuli may reach the brain in a relatively short time, such as 25 ms (Libet et al., 1967), while the brain may take a long time, more than 230 ms (Gomes, 1998) at least, to perceive it consciously. 5.1.3. Masking of the first stimulus The findings of Libet et al. (1967) indicate that the first stimulus used in a backward-masking paradigm seems to reach the cerebral cortex before the second stimulus is presented. This is because the ISI between the first and second stimuli, which was 40 ms in our experiments and 81 ms in that of MacIntyre and McComas (1996), is long enough for the first stimulus to reach the cerebral cortex. In contrast, these ISIs may be too short to produce conscious awareness (cf. Libet et al., 1992). The second stimulus must be presented during the course of information processing of the first stimulus, which has not yet been completed, thus, not allowing enough time for conscious awareness of the first stimulus to arise. A plausible explanation for backward masking has been proposed by Breitmeyer (Breitmeyer & Ganz, 1976; Breitmeyer & Ogmen, 2000) in terms of the notion of sustained and transient channels of sensory and perceptual systems. The sustained channel is thought to be responsible for processing relatively weak stim-

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uli (with a low threshold); this channel is slow to adapt and long-lasting as long as sensory inputs are applied. The transient channel is responsible for relatively strong stimuli (with a high threshold); this channel is fast to adapt and short-lived and responds to the onset and offset of sensory inputs. The notion of sustained and transient channels was hypothesised on the basis of the well-known neural functions of both rapidly adapting and slowly adapting sensory neurons in visual, auditory, and tactile modalities (Johansson & Vallbo, 1979; Sherrick & Cholewiak, 1986, Chap. 12). In backward masking, the sustained channel may be first activated by sensory inputs due to the first stimulus. Activation of the sustained channel is then inhibited or suppressed by the following activation of the transient channel when the second stimulus is presented. Such an inhibitory effect of the transient channel on the sustained channel may cause backward masking, that is, lack of awareness of the first stimulus. 5.2. Facilitation of motor response under backward masking In our results, simple RTs were shorter for the double (first plus second stimuli) than for the strong (strong stimulus alone) condition, despite conscious perception of the first stimulus being masked under the double condition. This implies that information processing for producing a motor response does not necessarily take place with (or after) conscious awareness of the given stimulus. Although the mechanisms underlying such a facilitation of a motor response are still open to question, it is plausible that the sensory inputs due to the first stimulus under the double condition may facilitate subsequent perceptual and/or motor processes, thus resulting in shortened RTs. 5.2.1. Facilitation of perceptual processes The Breitmeyer notion (Breitmeyer & Ganz, 1976; Breitmeyer & Ogmen, 2000) explains the backward-masking phenomenon, as described in the previous section. It is hypothesised that the sustained channel is activated by the first stimulus and then suppressed by the subsequent activation of the transient channel due to the second stimulus. The first stimulus probably activates the transient channel as well if the first stimulus is strong enough (such as the 1:2T and 2T in Experiment 2). Since the transient channel is fast to adapt and short-lived, it should be free from subsequent sensory inputs due to the second stimulus. The first stimulus can therefore facilitate the perceptual systems without any interruption by the second stimulus. The facilitated perceptual systems process sensory inputs from the second stimulus in a relatively short time, resulting in shorter RTs. In contrast, when the first stimulus is not strong enough to activate the transient channel, the perceptual systems are not well activated and fail to facilitate subsequent processing of the second stimulus. Such a situation can be seen in the results of Experiment 2. Shorter RTs appeared only for the 1:2T and 2T intensities but not for the T (i.e., threshold). This is because the T stimulus did not activate the transient channel, while the 1:2T and 2T did. To facilitate subsequent perceptual processes, a certain intensity level, higher than the 1:2T , may be needed.

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The notion of the temporal summation of sensory inputs can also provide a plausible explanation for the facilitation of perceptual processes. The temporal summation means successive and/or continuous sensory inputs on a particular receptive sensory neuron. It is well known that sensory sensitivity is increased by temporal summation and that sensory sensitivity increases as the stimulus duration increases within a range up to 80 ms (Saunders, 1975). In the backward-masking paradigm, the ISI between the first and second stimuli is usually shorter than 100 ms, namely, 40 ms in our experiments and 81 ms in that of MacIntyre and McComas (1996). Supposing that a pair of the first and second stimuli in the backward-masking paradigm forms a composite stimulus with a short gap of less than 80 ms, sensory sensitivity should increase. This may facilitate the perceptual processes for the second stimulus, thereafter facilitating the following motor responses. 5.2.2. Direct facilitation of motor-related processes The first stimulus may also directly facilitate the motor-related processes in parallel with the facilitation of perceptual processes. For such a parallel information processing, Hiramatsu et al. (1985) proposed a composite model of cognitive and motor-related processes. This model was based on their findings of both RT and P300, a type of event-related brain potentials (ERPs). The P300 generally indicates the nature of stimulus-evaluation processes, involving encoding, identification, and categorisation of a given stimulus (e.g., Kutas, McCarthy, & Donchin, 1977). In the Hiramatsu et al. model, an incoming stimulus is hypothesised to activate, in parallel, both the cognitive processes (such as stimulus identification, stimulus evaluation, decision making, and updating cognitive contexts) and motor-related processes (such as response preparation, response selection, and response execution). A likely cross-talk between the cognitive and motor-related processes is mediated by a hypothesised organising system. Relationships between the cognitive and motor-related processes have often been examined by comparing the RT and the latency of P300 (e.g., Kutas et al., 1977; Pfefferbaum, Ford, Johnson, Wenegrat, & Kopell, 1983). It is generally suggested that the correlation between the RT and the P300 latency is susceptible to the performerÕs response strategy, which may focus on maximizing either the accuracy or the speed of the response. Nishihira et al. (1999) have recently shown that EMG activities arise before the onset of P300 under particular conditions and that the motorrelated processes can precede the completion of stimulus-evaluation processes. This indicates that a motor response can be executed before the given stimulus is evaluated. It is accordingly suggested that a given stimulus may facilitate both the perceptual/cognitive and motor-related processes simultaneously and that, even when the perceptual processes do not lead to conscious awareness, the motor response can be facilitated. 5.2.3. Motor preparation without conscious awareness of intention Regarding motor-related information processing and consciousness, Keller and Heckhausen (1990) have shown evidence for nonconscious motor preparatory processes. They examined the readiness potentials (RPs) arising from finger movements

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that were unintentionally performed during a counting task. The RP, a type of ERPs, usually arises 800 ms or much earlier (up to about 1500 ms) prior to the onset of EMG activities (e.g., Deecke, Grozinger, & Kornhuber, 1976). Therefore, the RP has long been dealt with as an indicator of motor preparatory processes in the brain. Keller and Heckhausen showed that the onset of RPs appeared at almost the same latency for both the intended and unintended finger movements. This suggests that motor preparatory processes generally commence without conscious awareness of the intention of performing a movement. Furthermore, because RPs usually arise at an early time ranging from some 800 ms to 1500 ms prior to the onset of EMGs, the motor preparatory processes in most voluntary movements probably precede conscious awareness of the intention of the movement execution. Under the backward-masking paradigm, the first stimulus may be detected with the absence of conscious awareness of sensing the stimulus and, nevertheless, may trigger the motor preparatory processes. The motor preparatory processes may occur without conscious awareness of the intention for a movement action. Despite such behavioural findings, the neural mechanisms mediating nonconscious detection of a stimulus and how such sensory inputs arising from the nonconsciously detected stimulus activate subsequent motor preparatory processes that are also commenced without awareness of intention are still far from clear. These respective issues on nonconscious detection and subsequent nonconscious motor activation should be further examined in future research. More importantly, the likely linkage between sensory inputs and motor preparation (or the transformation from sensory inputs to motor action, as suggested by Goodale, 1998) under the absence of conscious awareness should be intensively focused on in considering the likely mechanisms underlying the dissociation between perception and action.

6. Conclusion In the present review, we examined the literature on the empirical evidence for the likely dissociation between perception and action. Both brain-damaged patients, such as those suffering from blindsight and visual/tactile agnosia, and experimental findings concerning pointing movements in normal people in response to a nonconsciously perceived stimulus were examined. We then closely reviewed our series of three experiments using backward masking, in which the first (weak) and second (strong) stimuli were presented with a short ISI. In Experiment 1, we compared simple RTs under three stimulus conditions: weak alone (weak), strong alone (strong), and weak plus strong (double). The participants reported that they perceived only the strong stimuli but not the weak stimulus under the double condition, while the RTs were significantly shorter for the double condition than for the strong one. In Experiment 2, we manipulated the intensity of the first stimulus to be threshold (T ), 1:2T or 2T and that of the second stimulus to be 4T . The participants were unaware of the first stimulus at both T and 1:2T under the double condition, while the RTs under the double condition became shorter for both 1:2T and 2T , but not for T , than those under the strong condition. In Experiment 3,

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we tested three different ISIs (20, 40, and 60 ms) while maintaining the stimulus intensities at 1:2T and 4T for the first and second stimulus. The RTs appeared to become shorter as the ISI became longer. These results indicated that motor responses under the double condition may have been triggered by sensory inputs arising from the first stimulus, which was perceived without awareness. It is therefore suggested that a motor response under backward masking is dissociated in part from conscious perception and that both the perceptual and motor processes may take place not in a series but, rather, in parallel. On the basis of these findings, we discussed likely mechanisms underlying nonconscious perception and motor responses in terms of the notion of sustained and transient channels (Breitmeyer & Ganz, 1976; Breitmeyer & Ogmen, 2000). The first stimulus may activate the sustained channel and is then suppressed by the transient channel, which is activated by the second stimulus. This may cause backward masking. To achieve a motor response to a nonconsciously perceived stimulus, the transient channel activated by the first stimulus (when stronger than 1:2T ) may facilitate either the perceptual or motor-related processes or both, leading to shorter RTs. Furthermore, it is suggested that the RPs could arise without conscious intention of performing a motor response and that both the perceptual and motor-related processes can be executed without awareness. This implies that the dissociation between perception and action may be mediated by nonconscious information processing, which takes place for both perception and action.

Acknowledgements We are grateful to Dr. Shuji Mori and anonymous reviewers for their critical and insightful comments on the original manuscript. This study was supported in part by Grant-in-Aid for Scientific Research (C #13680039) from the Japan Society for the Promotion of Science.

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