Rostral Prefrontal Lesions Impair Prospective Memory Cue Detection, but Not Action-Intention Superiority
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Knowing Your Lines but Missing Your Cue: Rostral Prefrontal Lesions Impair Prospective Memory Cue Detection, but Not Action-intention Superiority Sharon Uretzky1* and Asaf Gilboa2,3* Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/22/12/2745/1770875/jocn.2010.21419.pdf by guest on 18 May 2021 Abstract ■ Prospective memory (PM) deficits are a common conse- underlying (implicit) representations of intentions to perform an quence of lesions to PFC, but their underlying neurocognitive action, Z. P. showed normal patterns of intention superiority ef- mechanisms and processes are poorly understood. Here, we fects (ISEs) for to-be-performed actions and an inhibition effect report on a patient, Z. P., who suffers from a chronic focal PM for prospective actions after they had been performed. Thus, this deficit, while other cognitive functions including memory are is the first report of a neuropsychological dissociation between intact. His lesion involves right polar PFC (Brodmannʼsareas preserved privileged representation of prospective intentions 10 and 9). Z. P. was very impaired on tasks that require detection and impaired detection of cues that support the opportune recov- of PM cues during an ongoing task. He was impaired regardless ery of PM. Our data are compatible with the “gateway hypothesis” of whether the PM cues involved effortful or nearly effortless de- of rostral PFC, but also suggest there are components that are tection on the part of controls. By contrast, on tasks that tap the unique to PM and that remain intact after lesions to this region. ■ INTRODUCTION focuses on the internal representations of intention for Prospective memory (PM) is a form of memory which en- action (Goschke & Kuhl, 1993). The former models focus ables the performance of future actions at certain future on the kinds of processes that allow prospective actions to times or future events (Harris, 1984). The use of this form be performed at the appropriate times, whereas the latter of memory is common and pertinent to many realms in models attempt to explain the manner in which prospec- daily life. tive actions gain precedence over other representations to allow them to interrupt ongoing behavior. Cognitive Mechanisms of Prospective Memory Monitoring and Cue Detection PM depends on complex neurocognitive processes which often involve the functioning of multiple neurocognitive There are two primary models describing how cues asso- domains, such as retrospective memory and execu- ciated with prospective intents activate PM representations. tive functions (Burgess & Shallice, 1997). However, neuro- One model suggests that prospective remembering is en- psychological studies have reported patterns of impaired abled by a monitoring mechanism that is activated when PM despite intact functioning on domains considered crit- an intention for action is created. This retention mechanism ical for its performance, suggesting it also relies on certain of the prospective intent requires attention and executive unique and dissociable neurocognitive underpinning resources. It monitors the environment strategically until (West, McNerney, & Krauss, 2007; Bisiacchi, 1996). the target event for action execution is encountered. The There are two dominant theoretical approaches that prospective mechanism signifies the target eventʼspres- describe the neurocognitive mechanisms underlying pro- ence (Smith, 2003; Burgess & Shallice, 1997) and inhibits spective remembering. One focuses on monitoring of the the competing on-line action schema in order to enable environment and cue detection (Einstein & McDaniel, execution of the prospective action schema (Burgess, Scott, 2005; Smith, 2003; Burgess & Shallice, 1997) and the other & Frith, 2003). A frequent empirical method to examine monitoring functioning in laboratory experiments is by using an on- 1National Institute for Rehabilitation of the Brain Injured, Haifa, going task during which prospective targets periodically Israel, 2Haifa University, Mount Carmel, Haifa, Israel, 3Rambam appear and should be responded to distinctively. For ex- Medical Center, Haifa, Israel ample, subjects perform an ongoing lexical decision task *Equal contribution. during which they are also required to respond every time © 2010 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 22:12, pp. 2745–2757 Downloaded from http://www.mitpressjournals.org/doi/pdf/10.1162/jocn.2010.21419 by guest on 25 September 2021 they identify a certain syllable (prospective target) inside different “scripts,” each comprised of a set of instructions the words on screen. to be performed in the future, and after learning them, are Research shows that adding the prospective task de- asked to perform only one. Before performing the script, mands attention resources, and thus, results in a slower they are given a lexical decision task containing words that response time on the ongoing task (Smith, 2003). appeared in both scripts. Although both scripts are mem- A different account of prospective cue detection (Einstein orized to the same extent, RTs for words associated with & McDaniel, 2005) suggests that when intents for action a prospective intention are faster than RTs for words not are formed, an association between the action and the related to the prospective intention. This suggests an ele- cue for action performance is encoded. When the cue rep- vated activation level and resultant privileged processing resenting the target event is identified, the association for representations of the intention for action (Marsh, Downloaded from http://mitprc.silverchair.com/jocn/article-pdf/22/12/2745/1770875/jocn.2010.21419.pdf by guest on 18 May 2021 automatically activates the intention for action, which be- Hicks, & Bink, 1998). A related finding is that RTs for items comes conscious (Moscovitch, 1994). It is a reflexive direct associated with an already executed prospective intention retrieval operation that does not demand attentional re- are slower than RTs for items associated with nonprospective sources. This theory mainly explains event-based rather items in long-term memory, suggesting an inhibition of ac- than time-based PM. tivation of performed actions (Marsh et al., 1998). Typical experiments examining this theory are similar to the abovementioned paradigm, in that subjects perform an Neuropsychology of Prospective Memory ongoing task during which prospective targets may sporad- ically appear and should be responded to. The primary dif- Most of the research into PM impairment has dealt with ference is that prospective targets, such as syllables, are not populations suffering from general cognitive decline, such the primary focus of the ongoing task, which results in slower as aging, dementia, traumatic brain injury, or multiple reaction times (RTs) during lexical decisions, as predicted sclerosis (e.g., Kardiasmenos, Clawson, Wilken, & Walllin, by the active monitoring hypothesis. By contrast, when the 2008; Troyer & Murphy, 2007; Umeda, Nagumo, & Kato, targets are a salient part of the focus of the ongoing task 2006; Worthington, 1999). Deficits have generally been as- (e.g., a word in the lexical decision task), spontaneous as- cribed to attentional/executive dysfunction, which is sociative processes contribute more to the activation of usually ascribed to prefrontal cortex (PFC) or its connec- the prospective intention and little cost in RTs is observed. tions with subcortical structures. However, because other The “multiprocess theory” suggests that cue detec- cognitive domains that support PM are often also affected tion during prospective remembering relies, to different by these conditions, the specificity of the relationship to degrees, on both types of processes. The relative promi- the prospective components could not be determined. nence of more controlled versus more automatic processes Neuropsychological case studies of patients with promi- varies under different conditions depending on a variety nent PM impairment generally pointed to different aspects of variables. Some of the variables are related to the char- of PFC including medial PFC (Cockburn, 1995), orbito- acter of the task (e.g., the distinctiveness of the target event, frontal PFC (Worthington, 1999), or PFC nonspecifically the type of processing necessary to identify it) and some (Bisiacchi, 1996). West et al. (2007) have implicated white to individual differences (Einstein & McDaniel, 2005; matter and brain stem abnormalities, which could lead McDaniel & Einstein, 2000). to a disconnection syndrome with a PM dysfunction. In some of these cases, PM impairment appeared alongside more general executive impairment (Worthington, 1999; Intention for Action Representation Cockburn, 1995) and, in one case, alongside partial work- A second approach to PM focuses on the uniqueness of ing memory (WM) impairment (West et al., 2007). memory representation rather than on the prospective re- One prominent neuropsychological theory of PM spe- trieval process. It has been suggested that representations cifically implicates the rostral PFC (roughly corresponding of action intents within retrospective memory have an ele- to Brodmannʼs area 10) as critical to maintaining intention vated activation level and, as a result, are more salient com- over time and interference (Burgess, Simons, Dumontheil, pared to other representations. This saliency mediates a & Gilbert, 2005). By this view, primarily supported by privileged access to consciousness, which allows action