Author's personal copy Priming 1055 Priming R Henson , MRC Cognition and Brain Sciences Unit, to complete the stem with the first word that comes to Cambridge, UK mind. Priming is indexed by the increased probability ã of completing stems with studied words, relative to 2009 Elsevier Ltd. All rights reserved. the baseline probability of completing the stems when those words were not studied. Importantly, partici- pants normally show this priming without reporting Introduction any conscious reference to the prior study phase. Priming refers to a change in behavioral response to a Neuropsychological Evidence stimulus, following prior exposure to the same, or a related, stimulus. Examples include faster reaction When this task is given to amnesic patients, they times tomake a decision about the stimulus, a bias typically show priming of equivalent magnitude to controls. However, when the instructions at test are to produce that stimulus when generating responses, or the more accurate identification of a degraded changed, so that participants are asked to use the version of the stimulus. From the memory perspec- stems explicitly to recall studied words (‘word-stem tive, the most exciting aspect to priming concerns cued recall,’ a ‘direct’ version of the task), amnesic evidence that it can occur in the absence of conscious patients typically perform worse than controls memory for the prior exposure (an example of so- (Figure 1(b)). This dissociation is appealing because called ‘implicit’ or ‘nondeclarative’ memory). For in- the stimuli are kept constant across the indirect and direct versions of the task; all that differs are the stance, amnesic patients typically show intact levels of priming, despite their impairments in conscious instructions. While amnesic patients are also known (‘explicit’ or ‘declarative’) memory. Evidence like to have sparing of other forms of memory, such as motor skill-learning, the intriguing aspect of priming this led to the proposal that the brain regions support- ing priming are different from the medial temporal is that it can occur after a single stimulus presentation lobe (MTL) regions believed to support declarative (‘one-shot learning’), rather than requiring sustained memory. Indeed, it is often assumed that priming is training. Furthermore, a few patients with more pos- the by-product of prior processing of a stimulus, that terior lesions (e.g., in occipital cortex) have shown the is, arising from plasticity in multiple cortical regions reverse pattern of impaired word-stem completion for whose primary role is perceptual/conceptual proces- visually studied words (indirect test), despite intact performance on a recognition memory test (direct sing. As such, priming is likely to be one of the most basic expressions of memory, influencing how we test). This double dissociation between the two perceive and interpret the world. types of memory test is strong support for different memory systems underlying priming and declarative memory. Further support comes from reports that A Working Example word-stem completion priming is less susceptible Priming can be measured using a range of different than is cued recall to the effects of healthy aging, stimuli and tasks. To illustrate the breadth of neuro- and to some dementias like Alzheimer’s disease. scientific data on priming, we initially focus on one Psychological Evidence specific paradigm – the word-stem completion paradigm – which has provided some of the most This dissociation of priming from declarative memory convincing evidence that priming involves memory following brain damage is supported by functional systems, and associated brain regions, that differ dissociations between direct and indirect versions of from those involved in declarative memory. In the the word-stem completion paradigm in healthy indi- ‘study’ phase of this paradigm, participants perform viduals. For example, performance on the direct an incidental task on a list of words (normally un- version (word-stem cued-recall) is higher when the aware that their memory for these words will be corresponding words are generated from semantic tested). At some time later, they are presented with cues at study relative to when they are simply read, three letters that form the start of words (word-stems) yet performance on the indirect version (word-stem (see Figure 1(a)). Some of these stems can be com- completion) is higher when the words are read relative pleted with the words from the study phase, though in to being generated from cues. Similarly, presenting the ‘indirect’ version of this task, participants are not words auditorily rather than visually at study tends informed of any relationship between this test phase to impair performance on visual word-stem comple- and the previous study phase. They are simply asked tion to a greater extent than on visual word-stem cued Encyclopedia of Neuroscience (2009), vol. 7, pp. 1055-1063 Author's personal copy 1056 Priming Study phase Amnesics Controls MOTEL (Prime) 80 70 Test phase 60 MOT-? GAR-? 50 (Primed) (Unprimed) 40 30 Indirect version (completion): % completed 20 ‘complete with the first word coming to mind’ 10 Direct version (cued-recall): 0 ‘complete with a word from the study phase’ ab Completion Cued-recall Figure 1 (a) Schematic of the word-stem completion paradigm. (b) Performance of amnesic patients and matched controls on indirect (completion) and direct (cued-recall) versions of the task. (b) Reprinted with permission from Graf P, Squire LR, and Mandler G (1984) The information that amnesic patients do not forget. Journal of Experimental Psychology: Learning, Memory and Cognition 10: 164–178, APA publishers. recall, whereas use of a study task that engages seman- paradigm. These studies consistently found reduced tic versus phonological processing of words tends to hemodynamic responses in extrastriate visual cortex improve performance on word-stem cued recall to a for studied relative to unstudied word-stems (often in greater extent than on word-stem completion. The both direct and indirect versions of the task). This reduced performance found on word-stem completion reduction is attributed to ‘more efficient’ or ‘facili- when words are generated or heard at study, rather tated’ visual processing of the stems corresponding to than read, suggests that a component of priming in this studied words, owing to the prior exposure to those task relates to the visual overlap between words and words. Similar reductions have also been found in a their stems, or more precisely, to overlap in the pro- number of regions including left inferior temporal and cesses involved in visual word reading. left inferior frontal cortices. Given that these regions Nonetheless, though dissociations have been found are also generally activated by the task (e.g., vs. passive between direct and indirect tests of memory, care must fixation), the reductions are consistent with facilitated be taken when using performance on indirect tests as a processing within a language-related network that is pure measure of implicit memory: even though an engaged when reading words and completing word- indirect memory test does not refer participants to stems, possibly including phonological, lexical, and previous encounters with stimuli, participants may semantic processes. voluntarily, or involuntarily, recollect such encounters. Some imaging studies have also reported hemo- For example, some participants may guess the relation- dynamic increases in MTL cortices, even in indirect ship between the study and test phase of a word-stem versions of the task. This illustrates the problem high- completion task, and hence attempt to recall studied lighted earlier that explicit memory may contaminate items in order to complete the stems. Moreover, even if indirect tasks. In particular, even if this explicit mem- a completion comes to mind involuntarily, participants ory is involuntary and does not affect the behavioral may subsequently recognize that word as having come response, the poor temporal resolution of hemo- from the study phase. Though the latter eventuality dynamic imaging techniques means that imaging data may not affect behavioral measures of priming, it is may include explicit memory processes arising sub- important when measuring the neural correlates of sequent to that response. More recent imaging experi- priming, as discussed in the next two sections. As a ments have therefore used variants of the word-stem consequence, considerable effort has been devoted to completion paradigm that attempt to minimize con- developing methods that minimize the contribution of tamination by explicit memory. For example, partici- explicit memory to priming. pants can be asked to complete stems with words from the study phase (i.e., word-stem cued recall), Neuroimaging Evidence but if they cannot, they are asked to produce the Some of the first positron emission tomography (PET) first word coming to mind. Having produced a com- and functional magnetic resonance imaging (fMRI) pletion (through either approach), they then indicate studies of priming used the word-stem completion whether they remember that word from the study Encyclopedia of Neuroscience (2009), vol. 7, pp. 1055-1063 Author's personal copy Priming 1057 phase. The critical trials used to isolate the neural were completed with a studied word and that word correlates of priming are those stems completed was indicated as studied), unlike in MTL cortex, with studied words but which participants indicated where greater activity was found for remembered they did not remember. These trials are likely to trials relative to primed trials (suggesting that explicit provide a purer measure of implicit memory (despite memory had been successfully minimized in primed occurring in the context of a direct memory task). trials). Furthermore, the reductions for primed and When compared to a baseline condition (stems that remembered versus baseline trials in these regions did not correspond to studied words, but which were also found when using an indirect version of were completed with a word that was correctly indi- the task akin to the standard word-stem completion cated as unstudied), event-related fMRI has repli- task.