340 PHAN ET AL. functional rol for the basal gangli th MPFC.whileco y-bound mot ona s specif wit y en in der who have neuronathology y in their basal ganglia which r its this fr have impairments in recognizing facial expressions of fewer than 30%and 20%res F1g.2B). disgust compared to other emotions.The activations Instead,fear studies engage the amygdala robustly seen in the b respor to sgust may (over 60%frequency:d ussed earlier) Additionallv represent a state prepar by aw passive emotional co nditions witho e.g.,Emo et al 1998)With its know a functions.the basal ganglia may also serv to coordi. pu d nate appropriate action responses to stimuli that un- nections to s ubcortical limbic structur the MPEC oleasant (inducing disgusting).or pleasing (promoting and Acc could serve as ton-dowr modulators of in. nappiness),in at and gui e org towa hdraw)(Pank tense emotional responses,especially those generated by the amygdala.Several lines of evidence support sepp such an interpretation. al studies to be in fea condi 3.Regions Associated with Induction Methoo 1994.H ti 3.1 Regions involved in with and MPFC (Mor etal.1993). s in the hu an rostral MPFC also lead to socially inappropriate ex l tasks with ically engaged the AcC as compared to passive pressions of emotions and impairments in making ad- emo tageous personally relevant decisions (Damasio tional conditions (36 vs 12%.respectively:X 3.52. 994 ve proces ng of emo P=0.06) Earlier,when discussing the sugge nndings of the MPFC act with b ion and h s,we hypo ith tho dala in the of the bercrombie er al.1996).Our group has found that al task ct by cog nitive Demand).and interpreted that the MPFC may activity is the amygdaloid region is attenuated while have a general role in emotional proce the MPFC and cingulate sulcus are activated during a g.We spe ulated that the MPFC may respond to cognitive cognitive appraisal condition of aversive as versus pas ve view ylor et a ubmitted).A pects that are pot ng)(T ti y,de sLs th he am motional tasks and therefore are ent both in the nd Raichle 1008)one alterna studies with Cognitive Demand and in the studies with tive hynoth sis of thes e reciprocal findings is that lim- bic structures,like the amygdala,are more likely to Emotion alone.However,based on this analysis,when respond to stimuli that are more emotive at a sen cognitive comp ents explicit to an e emot ona sory/pe eptua recogniti level,and are ess likely to be engaged (e.g.,gen 1 cogni or to cogn motion rendering these task in the with Cognitive d emotions 31 Demand e1999 1997 it a ars that the ACC is re cruted.Therefore.the ACCad may interactwith the 32 Recall an th MPFC to regulate terconnected cog gnitive and emo- conditi ng on v it ly laden ev the A MDE ired e plicit intensive nitive effort Accordin xtensive co tions to subcortical limbic structures the recollection/recall induction of emotion specifically constitute both the heteromodal ass iation cortex and activated the anterior cingulate; 50%of recall in- and therefore comprise dies reporte AC activat ns,versus a pla rar sition and interaction zone between a studie oe C08 pect 05 also have additional of th A motional mo this tively der anding er onal tasks.and therefore this emotion interaction.As noted above.conditions with association suggests that recalled emotions are cogni- and without Cognitive Demand equally activate the tively elicited.as noted by Reiman et a/(1997)and functional role for the basal ganglia in processing dis￾gust, consistent with observations that patients with Huntington’s disease and obsessive-compulsive disor￾der, who have neuropathology in their basal ganglia, have impairments in recognizing facial expressions of disgust compared to other emotions. The activations seen in the basal ganglia in response to disgust may represent a state of preparedness triggered by a warn￾ing stimulus to process emotionally salient information (Sprengelmeyer et al., 1998). With its known motor functions, the basal ganglia may also serve to coordi￾nate appropriate action responses to stimuli that un￾pleasant (inducing disgusting), or pleasing (promoting happiness), in nature, and guide the organism towards a desired goal (e.g., to approach or withdraw) (Pank￾sepp, 1998). 3. Regions Associated with Induction Method 3.1 Regions involved in emotion induction with and without cognitive demand. This meta-analysis found that emotional tasks with cognitive components specif￾ically engaged the ACC as compared to passive emo￾tional conditions (36 vs 12%, respectively; X2 3.52, P 0.06). Earlier, when discussing the findings of the MPFC activation with both Emotion
Cognition and Emotion alone tasks, we hypothesized that activations seen in the MPFC are driven by the general component of the emotional task (e.g., with little impact by Cog￾nitive Demand), and interpreted that the MPFC may have a general role in emotional processing. We spec￾ulated that the MPFC may respond to cognitive as￾pects that are potentially common across various emo￾tional responses (e.g., attention to emotion, appraisal or interpretation of emotion), which are implicit to the emotional tasks and therefore are present both in the studies with Cognitive Demand and in the studies with Emotion alone. However, based on this analysis, when the cognitive components are explicit to an emotional task (e.g., gender identification, recognition/encoding or rating of emotional stimuli, biographical recall of emotion) rendering these task in the “with Cognitive Demand” category, it appears that the ACC is re￾cruited. Therefore, the ACCad may interact with the MPFC to regulate interconnected cognitive and emo￾tional tasks, depending on whether the cognitive com￾ponent is implicit or explicit to that emotional re￾sponse. Together, the rostral ACC and MPFC, with extensive connections to subcortical limbic structures, constitute both the heteromodal association cortex and paralimbic cortex respectively, and therefore comprise a plausible transition and interaction zone between affective and cognitive processing. The MPFC and ACCad may also have additional emotional modulatory functions from this cognitive￾emotion interaction. As noted above, conditions with and without Cognitive Demand equally activate the MPFC, while cognitively-bound emotional tasks specif￾ically engaged ACC. While most Individual Emotions activate both the MPFC and ACC, one exception in￾volves fear, which recruits this region at frequencies fewer than 30% and 20% respectively (see Fig. 2B). Instead, fear studies engage the amygdala robustly (over 60% frequency; discussed earlier). Additionally, passive emotional conditions without Cognitive De￾mand (e.g., Emotion alone) activate the amygdala more often than cognitive emotional tasks. Given their pu￾tative affective-cognitive functions and reciprocal con￾nections to subcortical limbic structures, the MPFC and ACC could serve as top-down modulators of in￾tense emotional responses, especially those generated by the amygdala. Several lines of evidence support such an interpretation. From animal studies, the amygdala has been shown to be critical in fear condi￾tioning (LeDoux, 1994). However, one can prolong the extinction of this conditioned fear by ablation of the MPFC (Morgan et al., 1993). Lesions in the human rostral MPFC also lead to socially inappropriate ex￾pressions of emotions and impairments in making ad￾vantageous personally relevant decisions (Damasio, 1994), suggesting a lack of cognitive processing of emo￾tionally “loaded” situations. Furthermore, glucose me￾tabolism in the MPFC is strongly inversely associated with the glucose metabolic rate of the amygdala (Am￾bercrombie et al., 1996). Our group has found that activity is the amygdaloid region is attenuated while the MPFC and cingulate sulcus are activated during a cognitive appraisal condition of aversive visual stimuli (versus passive viewing) (Taylor et al., submitted). Ad￾ditionally, deactivation of the amygdala has been ob￾served in several tasks that involve higher cognitive processing (Drevets and Raichle, 1998). One alterna￾tive hypothesis of these reciprocal findings is that lim￾bic structures, like the amygdala, are more likely to respond to stimuli that are more “emotive” at a sen￾sory/perceptual level, and are less likely to be engaged by cognitively demanding emotional tasks, or to cogni￾tively elicited emotions (Reiman et al., 1997; Teasdale et al., 1999). 3.2 Recall induction and the anterior cingulate. Similar to conditions with Cognitive Demand, those which induced emotions by evoking memories or imag￾ery of personally relevant affectively laden events re￾quired explicit intensive cognitive effort. Accordingly, the recollection/recall induction of emotion specifically activated the anterior cingulate; 50% of recall in￾duction studies reported ACC activations, versus 31% and 0% of visual and auditory induction studies, respectively (X2 5.96, P 0.05). As described above, recruitment of the ACC was specific to cogni￾tively demanding emotional tasks, and therefore, this association suggests that recalled emotions are cogni￾tively elicited, as noted by Reiman et al. (1997) and 340 PHAN ET AL.