Negative priming

• Dr. Steven P. Tipper, Psychology, University of Wales, Bangor, UK

• Mr. Bruce Weaver, Northern Ontario School of Medicine, Thunder Bay, ON, Canada

Figure 1: In order to grasp a particular cup, one must inhibit the internal representations of competing cups, and not allow them to capture control of action.

In the complex environments we inhabit, a vast amount of information bombards our senses. But in order to achieve goals, we must selectively attend to a limited amount of that information. For example, consider the simple task of grasping the cup indicated with an arrow in Figure 1. To achieve this goal, one must ignore the other cups and not allow them to capture control of action.

This process of ignoring is not without consequences. After a person has ignored a stimulus, processing of that ignored stimulus shortly afterwards is impaired. This experimental effect has been termed negative priming (Tipper, 1985).

An example

Consider List A in Figure 2. The task is to go down the list naming the color of the ink as quickly as possible while ignoring the words. Notice that this is quite difficult. Why? Because the extremely complex process of reading words has been automated by the brain such that even when one tries to ignore the word "RED" (for the first item), it is still processed, and it activates a response that competes with the correct response to the ink—"BLUE".

Figure 2: Illustration of negative priming using Stroop color words. Lists A and B show the Control and Ignored Repetition conditions respectively.

Now name the ink colors in List B. You might notice that List B seems a little more difficult than List A, even though you had some practice at the task when naming the colors in List A. In experiments with accurate timing of responses, this slowing has been confirmed numerous times (e.g., Dalrymple-Alford & Budayr, 1966; Pritchard & Neumann, 2004; Tipper, Bourke, Anderson, & Brehaut, 1989). The slower response time to name the ink colors in List B is an example of negative priming.

Why is it more difficult to read List B than List A? In List A (the Control condition), notice that for each stimulus, neither the color word nor the ink color have any overlap with the preceding item. For example, the first stimulus word is RED and the ink color to be named is BLUE (RED); and the second stimulus word is YELLOW and the ink to be named is PURPLE (YELLOW). In List B, however, there is a relationship between the ignored color word in one stimulus, and the to-be-named ink color in the next stimulus: That is, they are the same. For example, the first word is BLUE and the ink is GREEN (BLUE), while the second word is RED, but the ink color to be named is BLUE (RED), and so on down the list. Therefore in List B, negative priming emerges, because for each stimulus, people have to name a color that is the same as the ignored word in the previous display. (Lists A & B are examples of the Control and Ignored Repetition conditions respectively.)

Alternative accounts of negative priming

The inhibition account

This is the original account of negative priming (Tipper, 1985; Neill, 1977). As noted earlier, our senses are constantly bombarded with stimuli. The brain processes much of this information rapidly in parallel, and multiple sources of information can compete for the control of action. In Figure 2, for example, the words are processed even though they are irrelevant to the task of naming the ink color, and it takes effort to prevent response to them. One means by which such selection can be achieved is via inhibition of the internal representations of the competing stimuli. In this example, inhibition of the representations of the distracting color words enables responses to the attended ink colors.

The negative priming effect is one means of glimpsing this inhibitory process. It can be explained as follows. When a stimulus such as a picture of a DOG is viewed, it activates representations in the brain as part of the object recognition process. If the picture of the DOG has to be identified shortly afterwards, it is assumed that the same representations are required to process it. Because those representations are already active, the second processing of the stimulus is facilitated, and recognition of the dog image is quicker. However, if the internal representations of competing distractor stimuli have to be inhibited during selection of a target stimulus, then the opposite effect should be observed: i.e., a negative priming effect should result. For instance, if you have to actively ignore the picture of a dog while trying to identify some other stimulus, the internal representations of DOG will be inhibited. On the next trial, if you now have to identify a picture of a DOG, you will need access to the previously inhibited representations. But access to those representations will slow response relative to baseline conditions, because they were recently inhibited. Hence negative priming will be observed. In terms of Figure 2, you are slower naming the ink colors in List B because the color name you are trying to produce was the word inhibited while responding to the immediately previous item.

Episodic retrieval accounts

Episodic retrieval accounts argue that negative priming does not reflect inhibitory mechanisms of selective attention, but instead reflects memory processes. Currently, there are two main variants of the episodic retrieval account.

• Neill's version. According to Neill, Valdes, and Terry (1995), during processing of the initial (prime) display, the ignored stimulus (e.g., a picture of a DOG) is given a memory tag describing its status—e.g., an "ignore me" or "do not respond" tag. In the subsequent (probe) display when the previously ignored stimulus is presented as a to-be-attended target, the prior processing episode involving this stimulus is retrieved. Because the retrieved tag is "ignore me" or "do not respond", this causes confusion with the current requirement to respond to the picture of DOG, hence slowing down response.

• Prime-response retrieval model. According to a more recent version of the episodic retrieval account (Mayr & Buchner, 2006), the probe display in the ignored repetition condition triggers retrieval of the response associated with the prime display target. And because that response is incompatible with the required response for the probe display, performance is impaired. The best evidence for this model is the finding that on error trials, incorrect repetitions of the prime display target response are over-represented in the ignored repetition condition relative to control. In terms of Figure 2, for example, this model predicts that incorrect repetitions of the ink color from the preceding item will happen more often in list B (IR) than A (Control).

An integrative model

In an attempt to resolve this debate, Tipper (2001) argued that memory must be involved in all priming effects. In priming tasks, we observe how viewing a stimulus at one time influences processing of the same (or a related) stimulus at a subsequent time. This requires a link between past and present, which is the very stuff of memory. However, it is also necessary to consider the neural processes that enable completion of the task on any individual trial. In Figure 2, for example, how is it that people can so accurately and rapidly name the ink color, when clearly the color word is processed and competes for the control of action? Simply saying that the color word is tagged "do not respond", or that the probe triggers retrieval of the prime response does not describe the specific mechanism(s) of selection.

These selection processes must involve neural excitation and inhibition states that enable action to be selectively directed towards the correct object. And it is these specific selection processes that can be reinstated at a later time. Therefore, negative priming most likely reflects retrieval, not of abstract tags, but of specific prior processing states: The inhibitory feedback system used to suppress response to the distractor is retrieved or reactivated when the object is re-encountered, and slows current processing. Of course, whether an account of negative priming integrating both memory and inhibition processes will prove sufficient remains to be seen, as this debate continues with a range of sophisticated accounts attempting to deny a role for inhibition (e.g., Milliken, Joordens, Merikle, & Seiffert, 1998).

Properties of negative priming

The properties we list here are described from the point of view of the inhibition account of negative priming. We acknowledge that proponents of other accounts would use different terminology in line with their views.

• Semantic inhibition. The inhibition revealed via negative priming appears to be associated with deep level object identity, and can spread to related objects. For example, if a competing picture of a DOG is ignored, subsequent response to the word "DOG" is slowed. There is no physical relationship between the picture and word representing DOG, and therefore the inhibition must be at a deep semantic level. Furthermore, ignoring a picture of a DOG produces subsequent slowing when responding to CAT; and ignoring a word in one language (e.g., the Spanish word PERRO) can impair subsequent processing of the same word in a different language (DOG) (Neumann, McCloskey, & Felio, 1999). Such findings suggest that the inhibition can spread through semantic networks (Houghton & Tipper, 1994), and are not easily accommodated in episodic retrieval models.
• Object-based inhibition. Many of the objects we interact with move. For example, when meeting a friend at the airport, we search for them among a number of other moving individuals. How can we select and track a moving target from amongst moving distractors? It appears that the inhibition can be associated with moving objects, moving through space as the object moves even if the object is not visible at some times as it moves behind obstacles (Tipper, Brehaut, & Driver, 1990). Similar ideas of inhibition associated with objects were subsequently proposed for Inhibition of Return and Multiple Object Tracking.
• Action-based inhibition. The majority of experiments in psychology are carried out in conditions that are somewhat dissimilar to our real-world interactions with objects. That is, to achieve the necessary high levels of control when presenting stimuli and recording responses, visual inputs are often presented on flat 2D computer displays, and responses are often key-presses rather than direct responses toward the stimuli themselves. However, inhibition associated with competing distracting stimuli, observed via negative priming, can also be observed when people are reaching directly for objects in more real-world settings. Interestingly, the level of inhibition associated with the distracting stimulus is determined by the relationship between that stimulus and the responding hand, reflecting an action-based internal representation. As can be appreciated from Figure 1, irrelevant distractors closest to the responding hand compete most vigorously for the control of action, and hence require greater inhibition as revealed via increased negative priming effects (Tipper, Lortie, & Baylis, 1992).
• Individual differences. It has been suggested that different populations have different levels of inhibitory control, and that this can be revealed via negative priming. For example, individuals with schizophrenia, or schizotypal tendencies, have more difficulty ignoring irrelevant distracting information, and also exhibit reduced levels of negative priming (Beech, Powell, McWilliams, & Claridge, 1989). Reduced negative priming has also been observed in patients with Alzheimer’s disease (Vaughan, Hughes, Jones, Woods, & Tipper, 2006), depression (MacQueen, Tipper, Young, Joffe, & Levitt, 2000), and in the elderly (Verhaeghen & de Meersman, 1998; but see also Gamboz, Russo, & Fox, 2002). This suggests that decline in inhibitory control is a general feature of many groups with reduced information processing efficiency.

Figure 3: Activation of left anterior temporal cortex (ATC) was correlated with identity-based negative priming. Activation associated with negative priming was also detected in supplementary eye field (SEF) and left inferior parietal cortex (IPL). (We thank Grieg de Zubricaray for providing this figure.)

• Neuroanatomy & inhibition. Inhibitory neural systems have been discovered and extensively analysed via studies with animals. Recording from single neurons has enabled a glimpse of the complex interplay between excitatory and inhibitory neurons (see neural inhibition). Studying inhibitory processes in intact humans is of course much more complex, requiring more indirect approaches such as negative priming. One of the key goals for future research will be to link negative priming to the neural systems that mediate inhibitory processes. First steps have been made utilizing brain imaging techniques and patients with focal lesions. For example, recent work suggests that inhibition associated with semantic properties of an object is mediated by left anterior temporal cortex, as shown in Figure 3 (de Zubicarray, McMahon, Eastburn, Pringle, & Lorenz, 2006). Also, there is increasing evidence that the prefrontal cortex plays an important role in inhibitory control systems. At present, it is not clear whether the critical areas are in the left or right frontal regions. Some evidence points to the left (McDonald et al., 2005) and some to the right (Stuss et al., 1999). But of course, inhibitory control systems will be goal-dependent, and different neural networks will be recruited for different tasks and stimulus domains. Additional recent work, for example, suggests that inhibition associated with shape or identity properties of an object is mediated bilaterally by the lingual gyri of posterior visual cortex (Vuilleumier, Schwartz, Duhoux, Dolan, & Driver, 2005). Therefore, variable data is to be expected from such a dynamic system.

References

• Beech, A., Powell, T., McWilliams, J., & Claridge, G. (1989). Evidence of reduced cognitive inhibition in schizophrenics. British Journal of Psychology, 28, 109-116.

• Dalrymple-Alford, E.C. & Budayr, B. (1966). Examination of some aspects of the Stroop color word test. Perceptual & Motor Skills, 23, 1211-1214.

• Gamboz, N., Russo, R. & Fox, E. (2002). Age differences and the identity negative priming effect: An updated meta-analysis. Psychology & Aging, 17, 525-531.

• Houghton, G. & Tipper, S.P. (1994). A model of inhibitory mechanisms in selective attention. In D. Dagenback and T. Carr (Eds), Inhibitory Processes of Attention, Memory and Language. Academic Press: Florida. pp 53-112.

• MacQueen, G.M., Tipper, S.P., Young, L.T., Joffe, R.T., & Levitt, A.J. (2000). Impaired distractor inhibition on a selective attention task in unmedicated, depressed subjects. Psychological Medicine, 30, 557-564.

• Mayr, S., & Buchner, A. (2006). Evidence for episodic retrieval of inadequate prime responses in auditory negative priming. Journal of Experimental Psychology: Human Perception and Performance, 32, 932-943.

• McDonald, C.R., Bauer, R.M, Filoteo, J.V., Grande, L., Roper, S.N., & Gilmore, R. (2005). Attentional inhibition in patients with focal frontal lobe lesions. Journal of Clinical and Experimental Neuropsychology, 27, 485-503.

• Milliken, B., Joordens, S., Merikle, P.M., & Seiffert, A.E. (1998). Selective attention: A reevaluation of the implications of negative priming. Psychological Review, 105, 203-229.

• Neill, W.T. (1977). Inhibition and facilitation processes in selective attention. Journal of Experimental Psychology: Human Perception & Performance, 3, 444-450.

• Neill, W.T., Valdes, L.A., & Terry, K.M. (1995). Selective attention and the inhibitory control of cognition. In F.N. Dempster & C.J. Brainerd (Eds.), New Perspectives on interference and inhibition in cognition. (pp. 207-261), New York: Academic Press).

• Neumann, E., McCloskey, M.S., & Felio, A.C. (1999). Cross-language positive priming disappears, negative priming does not: Evidence for two sources of selective inhibition. Memory & Cognition, 27, 1051-1063.

• Pritchard, V. E., & Neumann, E. (2004). Negative priming effects in children engaged in non- spatial tasks: Evidence for early development of an intact inhibitory mechanism. Developmental Psychology, 40, 191-203.

• Stuss, D.T., Toth, J.P., Franchi, D., Alexander, M.P., Tipper, S.P., & Craik, F.I.G. (1999). Dissociation of attentional processes in patients with focal frontal and posterior lesions. Neuropsychologia, 37, 1005-1027.

• Tipper, S.P. (1985). The negative priming effect: Inhibitory priming with to be ignored objects. The Quarterly Journal of Experimental Psychology, 37A, 571-590.

• Tipper, S.P., Bourke, T., Anderson, S. & Brehaut, J. (1989) Mechanisms of attention: A developmental study. Journal of Experimental Child Psychology, 48, 353-378.

• Tipper, S.P., Brehaut, J.C. & Driver, J. (1990) Selection of moving and static objects for the control of spatially directed action. Journal of Experimental Psychology: Human Perception and Performance, 16, 492-504.

• Tipper, S.P., Lortie, C. & Baylis, G.C. (1992) Selective reaching: Evidence for action centered attention. Journal of Experimental Psychology: Human Perception and Performance, 18, 891-905.

• Tipper, S.P. (2001). Does negative priming reflect inhibitory mechanisms? A review and integration of conflicting views. Quarterly Journal of Experimental Psychology, 54A, 321-343.

• Vaughan, F.L., Hughes, E.A., Jones, R.S.P., Woods, R.T., & Tipper, S.P. (2006). Spatial negative priming in early Alzheimer’s disease: Evidence for reduced cognitive inhibition. Journal of the International Neuropsychological Society, 12, 416-423.

• Verhaeghen, P. & De Meersman, L. (1998). Aging and the negative priming effect: A meta-analysis. Psychology and Aging, 13, 435-444.

• Vuilleumier, P., Schwartz, S., Duhoux, S., Dolan, R.,J., & Driver, J. (2005). Selective attention modulates neural substrates of repetition priming and “implicit” visual memory: Suppressions and enhancements revealed by fMRI. Journal of Cognitive Neuroscience, 17, 1245-1260.

• de Zubicarray, G., McMahon, K., Eastburn, M., Pringle, A., & Lorenz, L. (2006). Classic identity negative priming involves accessing semantic representations in the left anterior temporal cortex. Neuroimage, 33, 383-390.

Internal references

• Valentino Braitenberg (2007) Brain. Scholarpedia, 2(11):2918.

• William D. Penny and Karl J. Friston (2007) Functional imaging. Scholarpedia, 2(5):1478.

• Mark Aronoff (2007) Language. Scholarpedia, 2(5):3175.

• Howard Eichenbaum (2008) Memory. Scholarpedia, 3(3):1747.

• Zenon Pylyshyn (2007) Multiple object tracking. Scholarpedia, 2(10):3326.

• Peter Jonas and Gyorgy Buzsaki (2007) Neural inhibition. Scholarpedia, 2(9):3286.

• Almut Schüz (2008) Neuroanatomy. Scholarpedia, 3(3):3158.

• Marco M Picchioni and Robin Murray (2008) Schizophrenia. Scholarpedia, 3(4):4132.

See also

Attention, Inhibition, Inhibition of return, Priming

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Reviewed by: Anonymous

Accepted on: 2008-02-13 18:25:24 GMT