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Contents
Academic Editor
- Alberto Cabrera Zubizarreta
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[1]LaBar KS, Cabeza R. Cognitive neuroscience of emotional memory. Nature Reviews. Neuroscience. 2006; 7: 54–64. https://doi.org/10.1038/nrn1825.
[2]Cahill L, Uncapher M, Kilpatrick L, Alkire MT, Turner J. Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an FMRI investigation. Learning & Memory (Cold Spring Harbor, N.Y.). 2004; 11: 261–266. https://doi.org/10.1101/lm.70504.
[3]Hamann SB, Ely TD, Grafton ST, Kilts CD. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience. 1999; 2: 289–293. https://doi.org/10.1038/6404.
[4]Kensinger EA, Schacter DL. Neural processes supporting young and older adults’ emotional memories. Journal of Cognitive Neuroscience. 2008; 20: 1161–1173. https://doi.org/10.1162/jocn.2008.20080.
[5]Kilpatrick L, Cahill L. Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage. NeuroImage. 2003; 20: 2091–2099. https://doi.org/10.1016/j.neuroimage.2003.08.006.
[6]Murty VP, Sambataro F, Das S, Tan HY, Callicott JH, Goldberg TE, et al. Age-related alterations in simple declarative memory and the effect of negative stimulus valence. Journal of Cognitive Neuroscience. 2009; 21: 1920–1933. https://doi.org/10.1162/jocn.2009.21130.
[7]Ritchey M, Dolcos F, Cabeza R. Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. Cerebral Cortex (New York, N.Y.: 1991). 2008; 18: 2494–2504. https://doi.org/10.1093/cercor/bhm262.
[8]Kapur S, Craik FI, Tulving E, Wilson AA, Houle S, Brown GM. Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. Proceedings of the National Academy of Sciences of the United States of America. 1994; 91: 2008–2011. https://doi.org/10.1073/pnas.91.6.2008.
[9]Otten LJ, Henson RN, Rugg MD. Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. Brain: a Journal of Neurology. 2001; 124: 399–412. https://doi.org/10.1093/brain/124.2.399.
[10]Prince SE, Tsukiura T, Cabeza R. Distinguishing the neural correlates of episodic memory encoding and semantic memory retrieval. Psychological Science. 2007; 18: 144–151. https://doi.org/10.1111/j.1467-9280.2007.01864.x.
[11]Otten LJ, Rugg MD. Task-dependency of the neural correlates of episodic encoding as measured by fMRI. Cerebral Cortex (New York, N.Y.: 1991). 2001; 11: 1150–1160. https://doi.org/10.1093/cercor/11.12.1150.
[12]Prince SE, Daselaar SM, Cabeza R. Neural correlates of relational memory: successful encoding and retrieval of semantic and perceptual associations. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience. 2005; 25: 1203–1210. https://doi.org/10.1523/JNEUROSCI.2540-04.2005.
[13]Golby AJ, Poldrack RA, Brewer JB, Spencer D, Desmond JE, Aron AP, et al. Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain: a Journal of Neurology. 2001; 124: 1841–1854. https://doi.org/10.1093/brain/124.9.1841.
[14]Kennepohl S, Sziklas V, Garver KE, Wagner DD, Jones-Gotman M. Memory and the medial temporal lobe: hemispheric specialization reconsidered. NeuroImage. 2007; 36: 969–978. https://doi.org/10.1016/j.neuroimage.2007.03.049.
[15]Giovanello KS, Schnyer DM, Verfaellie M. A critical role for the anterior hippocampus in relational memory: evidence from an fMRI study comparing associative and item recognition. Hippocampus. 2004; 14: 5–8. https://doi.org/10.1002/hipo.10182.
[16]Jackson O, 3rd, Schacter DL. Encoding activity in anterior medial temporal lobe supports subsequent associative recognition. NeuroImage. 2004; 21: 456–462. https://doi.org/10.1016/j.neuroimage.2003.09.050.
[17]Park H, Rugg MD. Neural correlates of encoding within- and across-domain inter-item associations. Journal of Cognitive Neuroscience. 2011; 23: 2533–2543. https://doi.org/10.1162/jocn.2011.21611.
[18]Koutstaal W, Reddy C, Jackson EM, Prince S, Cendan DL, Schacter DL. False recognition of abstract versus common objects in older and younger adults: testing the semantic categorization account. Journal of Experimental Psychology. Learning, Memory, and Cognition. 2003; 29: 499–510. https://doi.org/10.1037/0278-7393.29.4.499.
[19]Murty VP, Ritchey M, Adcock RA, LaBar KS. Reprint of: fMRI studies of successful emotional memory encoding: a quantitative meta-analysis. Neuropsychologia. 2011; 49: 695–705. https://doi.org/10.1016/j.neuropsychologia.2011.02.031.
[20]Canli T, Desmond JE, Zhao Z, Gabrieli JDE. Sex differences in the neural basis of emotional memories. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99: 10789–10794. https://doi.org/10.1073/pnas.162356599.
[21]Kensinger EA, Garoff-Eaton RJ, Schacter DL. How negative emotion enhances the visual specificity of a memory. Journal of Cognitive Neuroscience. 2007; 19: 1872–1887. https://doi.org/10.1162/jocn.2007.19.11.1872.
[22]Mackiewicz KL, Sarinopoulos I, Cleven KL, Nitschke JB. The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103: 14200–14205. https://doi.org/10.1073/pnas.0601648103.
[23]Mickley Steinmetz KR, Kensinger EA. The effects of valence and arousal on the neural activity leading to subsequent memory. Psychophysiology. 2009; 46: 1190–1199. https://doi.org/10.1111/j.1469-8986.2009.00868.x.
[24]Rasch B, Spalek K, Buholzer S, Luechinger R, Boesiger P, Papassotiropoulos A, et al. A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106: 19191–19196. https://doi.org/10.1073/pnas.0907425106.
[25]Sergerie K, Lepage M, Armony JL. A process-specific functional dissociation of the amygdala in emotional memory. Journal of Cognitive Neuroscience. 2006; 18: 1359–1367. https://doi.org/10.1162/jocn.2006.18.8.1359.
[26]St Jacques PL, Dolcos F, Cabeza R. Effects of aging on functional connectivity of the amygdala for subsequent memory of negative pictures: a network analysis of functional magnetic resonance imaging data. Psychological Science. 2009; 20: 74–84. https://doi.org/10.1111/j.1467-9280.2008.02258.x.
[27]Talmi D, Anderson AK, Riggs L, Caplan JB, Moscovitch M. Immediate memory consequences of the effect of emotion on attention to pictures. Learning & Memory (Cold Spring Harbor, N.Y.). 2008; 15: 172–182. https://doi.org/10.1101/lm.722908.
[28]Dougal S, Phelps EA, Davachi L. The role of medial temporal lobe in item recognition and source recollection of emotional stimuli. Cognitive, Affective & Behavioral Neuroscience. 2007; 7: 233–242. https://doi.org/10.3758/cabn.7.3.233.
[29]Kensinger EA, Schacter DL. Retrieving accurate and distorted memories: neuroimaging evidence for effects of emotion. NeuroImage. 2005; 27: 167–177. https://doi.org/10.1016/j.neuroimage.2005.03.038.
[30]Kensinger EA, Corkin S. Two routes to emotional memory: distinct neural processes for valence and arousal. Proceedings of the National Academy of Sciences of the United States of America. 2004; 101: 3310–3315. https://doi.org/10.1073/pnas.0306408101.
[31]Sommer T, Gläscher J, Moritz S, Büchel C. Emotional enhancement effect of memory: removing the influence of cognitive factors. Learning & Memory (Cold Spring Harbor, N.Y.). 2008; 15: 569–573. https://doi.org/10.1101/lm.995108.
[32]Kensinger EA, Schacter DL. Amygdala activity is associated with the successful encoding of item, but not source, information for positive and negative stimuli. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience. 2006; 26: 2564–2570. https://doi.org/10.1523/JNEUROSCI.5241-05.2006.
[33]Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT. Activation likelihood estimation meta-analysis revisited. NeuroImage. 2012; 59: 2349–2361. https://doi.org/10.1016/j.neuroimage.2011.09.017.
[34]Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapping. 2009; 30: 2907–2926. https://doi.org/10.1002/hbm.20718.
[35]Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P. Minimizing within-experiment and within-group effects in Activation Likelihood Estimation meta-analyses. Human Brain Mapping. 2012; 33: 1–13. https://doi.org/10.1002/hbm.21186.
[36]SCOVILLE WB, MILNER B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry. 1957; 20: 11–21. https://doi.org/10.1136/jnnp.20.1.11.
[37]Papanicolaou AC, Simos PG, Castillo EM, Breier JI, Katz JS, Wright AA. The hippocampus and memory of verbal and pictorial material. Learning & Memory (Cold Spring Harbor, N.Y.). 2002; 9: 99–104. https://doi.org/10.1101/lm.44302.
[38]Parsons MW, Haut MW, Lemieux SK, Moran MT, Leach SG. Anterior medial temporal lobe activation during encoding of words: FMRI methods to optimize sensitivity. Brain and Cognition. 2006; 60: 253–261. https://doi.org/10.1016/j.bandc.2005.07.010.
[39]Kondo Y, Suzuki M, Mugikura S, Abe N, Takahashi S, Iijima T, et al. Changes in brain activation associated with use of a memory strategy: a functional MRI study. NeuroImage. 2005; 24: 1154–1163. https://doi.org/10.1016/j.neuroimage.2004.10.033.
[40]Hamann S. Cognitive and neural mechanisms of emotional memory. Trends in Cognitive Sciences. 2001; 5: 394–400. https://doi.org/10.1016/s1364-6613(00)01707-1.
Academic Editor
- Alberto Cabrera Zubizarreta
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, Sandra Azareli García Velázquez 2, Peter T. Fox Selby 1,2,3,4,51 Research Imaging Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229-3900, USA
2 Departamento de Neurología, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229-3900, USA
3 South Texas Veterans Health Care System, San Antonio, TX 78229-3900, USA
4 Departamento de Radiología, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229-3900, USA
5 Departamento de Psiquiatría, University of Texas Health Science Center at San Antonio, San Antonio, TX 78229-3900, USA
Abstract
Functional magnetic resonance imaging (fMRI) studies examining emotional memory encoding often use event-related designs with stimuli in the form of words or pictures. Prior research has suggested differential hemispheric specialization for these stimulus types, yet no meta-analysis has directly compared the neural systems involved in each.
A meta-analysis was conducted using peer-reviewed, event-related fMRI studies. The Activation Likelihood Estimation (ALE) method was applied via GingerALE software to compare brain activations associated with the encoding of affective visual stimuli presented as either words or photographs. Three contrasts were assessed: pictures > neutral + control, words > neutral + control, and overlap between both.
Picture stimuli elicited bilateral activation in the medial parahippocampus, while word stimuli produced left-lateralized activation in the lateral parahippocampus. The overlap analysis identified a shared region in the parahippocampal amygdala. All three contrasts revealed significant activations in key medial temporal lobe (MTL) regions involved in emotional memory, including the hippocampus and amygdala.
Both stimulus types engaged medial temporal networks specialized in emotional memory encoding. Word stimuli selectively activated regions lateralized to the left hemisphere, whereas picture stimuli produced bilateral activation with a leftward bias. This study provides the first meta-analytic evidence of a medial-lateral differentiation in the parahippocampal gyrus based on emotional stimulus type.
Keywords
- emotion
- emotional memory
- affective words
- affective pictures
- event-related fMRI
- funcitonal magnetic resonance imaging (fMRI)
- activation likelihood estimation (ALE)
- parahippocampal gyrus
- medial temporal lobe
- hemispheric lateralization
- coordinate-based meta-analysis
References
- [1]
LaBar KS, Cabeza R. Cognitive neuroscience of emotional memory. Nature Reviews. Neuroscience. 2006; 7: 54–64. https://doi.org/10.1038/nrn1825. - [2]
Cahill L, Uncapher M, Kilpatrick L, Alkire MT, Turner J. Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an FMRI investigation. Learning & Memory (Cold Spring Harbor, N.Y.). 2004; 11: 261–266. https://doi.org/10.1101/lm.70504. Cited within: 3Google Scholar - [3]
Hamann SB, Ely TD, Grafton ST, Kilts CD. Amygdala activity related to enhanced memory for pleasant and aversive stimuli. Nature Neuroscience. 1999; 2: 289–293. https://doi.org/10.1038/6404. - [4]
Kensinger EA, Schacter DL. Neural processes supporting young and older adults’ emotional memories. Journal of Cognitive Neuroscience. 2008; 20: 1161–1173. https://doi.org/10.1162/jocn.2008.20080. - [5]
Kilpatrick L, Cahill L. Amygdala modulation of parahippocampal and frontal regions during emotionally influenced memory storage. NeuroImage. 2003; 20: 2091–2099. https://doi.org/10.1016/j.neuroimage.2003.08.006. - [6]
Murty VP, Sambataro F, Das S, Tan HY, Callicott JH, Goldberg TE, et al. Age-related alterations in simple declarative memory and the effect of negative stimulus valence. Journal of Cognitive Neuroscience. 2009; 21: 1920–1933. https://doi.org/10.1162/jocn.2009.21130. - [7]
Ritchey M, Dolcos F, Cabeza R. Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. Cerebral Cortex (New York, N.Y.: 1991). 2008; 18: 2494–2504. https://doi.org/10.1093/cercor/bhm262. - [8]
Kapur S, Craik FI, Tulving E, Wilson AA, Houle S, Brown GM. Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. Proceedings of the National Academy of Sciences of the United States of America. 1994; 91: 2008–2011. https://doi.org/10.1073/pnas.91.6.2008. - [9]
Otten LJ, Henson RN, Rugg MD. Depth of processing effects on neural correlates of memory encoding: relationship between findings from across- and within-task comparisons. Brain: a Journal of Neurology. 2001; 124: 399–412. https://doi.org/10.1093/brain/124.2.399. - [10]
Prince SE, Tsukiura T, Cabeza R. Distinguishing the neural correlates of episodic memory encoding and semantic memory retrieval. Psychological Science. 2007; 18: 144–151. https://doi.org/10.1111/j.1467-9280.2007.01864.x. - [11]
Otten LJ, Rugg MD. Task-dependency of the neural correlates of episodic encoding as measured by fMRI. Cerebral Cortex (New York, N.Y.: 1991). 2001; 11: 1150–1160. https://doi.org/10.1093/cercor/11.12.1150. - [12]
Prince SE, Daselaar SM, Cabeza R. Neural correlates of relational memory: successful encoding and retrieval of semantic and perceptual associations. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience. 2005; 25: 1203–1210. https://doi.org/10.1523/JNEUROSCI.2540-04.2005. - [13]
Golby AJ, Poldrack RA, Brewer JB, Spencer D, Desmond JE, Aron AP, et al. Material-specific lateralization in the medial temporal lobe and prefrontal cortex during memory encoding. Brain: a Journal of Neurology. 2001; 124: 1841–1854. https://doi.org/10.1093/brain/124.9.1841. - [14]
Kennepohl S, Sziklas V, Garver KE, Wagner DD, Jones-Gotman M. Memory and the medial temporal lobe: hemispheric specialization reconsidered. NeuroImage. 2007; 36: 969–978. https://doi.org/10.1016/j.neuroimage.2007.03.049. - [15]
Giovanello KS, Schnyer DM, Verfaellie M. A critical role for the anterior hippocampus in relational memory: evidence from an fMRI study comparing associative and item recognition. Hippocampus. 2004; 14: 5–8. https://doi.org/10.1002/hipo.10182. - [16]
Jackson O, 3rd, Schacter DL. Encoding activity in anterior medial temporal lobe supports subsequent associative recognition. NeuroImage. 2004; 21: 456–462. https://doi.org/10.1016/j.neuroimage.2003.09.050. - [17]
Park H, Rugg MD. Neural correlates of encoding within- and across-domain inter-item associations. Journal of Cognitive Neuroscience. 2011; 23: 2533–2543. https://doi.org/10.1162/jocn.2011.21611. - [18]
Koutstaal W, Reddy C, Jackson EM, Prince S, Cendan DL, Schacter DL. False recognition of abstract versus common objects in older and younger adults: testing the semantic categorization account. Journal of Experimental Psychology. Learning, Memory, and Cognition. 2003; 29: 499–510. https://doi.org/10.1037/0278-7393.29.4.499. - [19]
Murty VP, Ritchey M, Adcock RA, LaBar KS. Reprint of: fMRI studies of successful emotional memory encoding: a quantitative meta-analysis. Neuropsychologia. 2011; 49: 695–705. https://doi.org/10.1016/j.neuropsychologia.2011.02.031. - [20]
Canli T, Desmond JE, Zhao Z, Gabrieli JDE. Sex differences in the neural basis of emotional memories. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99: 10789–10794. https://doi.org/10.1073/pnas.162356599. - [21]
Kensinger EA, Garoff-Eaton RJ, Schacter DL. How negative emotion enhances the visual specificity of a memory. Journal of Cognitive Neuroscience. 2007; 19: 1872–1887. https://doi.org/10.1162/jocn.2007.19.11.1872. - [22]
Mackiewicz KL, Sarinopoulos I, Cleven KL, Nitschke JB. The effect of anticipation and the specificity of sex differences for amygdala and hippocampus function in emotional memory. Proceedings of the National Academy of Sciences of the United States of America. 2006; 103: 14200–14205. https://doi.org/10.1073/pnas.0601648103. - [23]
Mickley Steinmetz KR, Kensinger EA. The effects of valence and arousal on the neural activity leading to subsequent memory. Psychophysiology. 2009; 46: 1190–1199. https://doi.org/10.1111/j.1469-8986.2009.00868.x. - [24]
Rasch B, Spalek K, Buholzer S, Luechinger R, Boesiger P, Papassotiropoulos A, et al. A genetic variation of the noradrenergic system is related to differential amygdala activation during encoding of emotional memories. Proceedings of the National Academy of Sciences of the United States of America. 2009; 106: 19191–19196. https://doi.org/10.1073/pnas.0907425106. - [25]
Sergerie K, Lepage M, Armony JL. A process-specific functional dissociation of the amygdala in emotional memory. Journal of Cognitive Neuroscience. 2006; 18: 1359–1367. https://doi.org/10.1162/jocn.2006.18.8.1359. - [26]
St Jacques PL, Dolcos F, Cabeza R. Effects of aging on functional connectivity of the amygdala for subsequent memory of negative pictures: a network analysis of functional magnetic resonance imaging data. Psychological Science. 2009; 20: 74–84. https://doi.org/10.1111/j.1467-9280.2008.02258.x. - [27]
Talmi D, Anderson AK, Riggs L, Caplan JB, Moscovitch M. Immediate memory consequences of the effect of emotion on attention to pictures. Learning & Memory (Cold Spring Harbor, N.Y.). 2008; 15: 172–182. https://doi.org/10.1101/lm.722908. Cited within: 3Google Scholar - [28]
Dougal S, Phelps EA, Davachi L. The role of medial temporal lobe in item recognition and source recollection of emotional stimuli. Cognitive, Affective & Behavioral Neuroscience. 2007; 7: 233–242. https://doi.org/10.3758/cabn.7.3.233. Cited within: 3Google Scholar - [29]
Kensinger EA, Schacter DL. Retrieving accurate and distorted memories: neuroimaging evidence for effects of emotion. NeuroImage. 2005; 27: 167–177. https://doi.org/10.1016/j.neuroimage.2005.03.038. - [30]
Kensinger EA, Corkin S. Two routes to emotional memory: distinct neural processes for valence and arousal. Proceedings of the National Academy of Sciences of the United States of America. 2004; 101: 3310–3315. https://doi.org/10.1073/pnas.0306408101. - [31]
Sommer T, Gläscher J, Moritz S, Büchel C. Emotional enhancement effect of memory: removing the influence of cognitive factors. Learning & Memory (Cold Spring Harbor, N.Y.). 2008; 15: 569–573. https://doi.org/10.1101/lm.995108. Cited within: 3Google Scholar - [32]
Kensinger EA, Schacter DL. Amygdala activity is associated with the successful encoding of item, but not source, information for positive and negative stimuli. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience. 2006; 26: 2564–2570. https://doi.org/10.1523/JNEUROSCI.5241-05.2006. - [33]
Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT. Activation likelihood estimation meta-analysis revisited. NeuroImage. 2012; 59: 2349–2361. https://doi.org/10.1016/j.neuroimage.2011.09.017. - [34]
Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Human Brain Mapping. 2009; 30: 2907–2926. https://doi.org/10.1002/hbm.20718. - [35]
Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P. Minimizing within-experiment and within-group effects in Activation Likelihood Estimation meta-analyses. Human Brain Mapping. 2012; 33: 1–13. https://doi.org/10.1002/hbm.21186. - [36]
SCOVILLE WB, MILNER B. Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry. 1957; 20: 11–21. https://doi.org/10.1136/jnnp.20.1.11. - [37]
Papanicolaou AC, Simos PG, Castillo EM, Breier JI, Katz JS, Wright AA. The hippocampus and memory of verbal and pictorial material. Learning & Memory (Cold Spring Harbor, N.Y.). 2002; 9: 99–104. https://doi.org/10.1101/lm.44302. Cited within: 1Google Scholar - [38]
Parsons MW, Haut MW, Lemieux SK, Moran MT, Leach SG. Anterior medial temporal lobe activation during encoding of words: FMRI methods to optimize sensitivity. Brain and Cognition. 2006; 60: 253–261. https://doi.org/10.1016/j.bandc.2005.07.010. - [39]
Kondo Y, Suzuki M, Mugikura S, Abe N, Takahashi S, Iijima T, et al. Changes in brain activation associated with use of a memory strategy: a functional MRI study. NeuroImage. 2005; 24: 1154–1163. https://doi.org/10.1016/j.neuroimage.2004.10.033. - [40]
Hamann S. Cognitive and neural mechanisms of emotional memory. Trends in Cognitive Sciences. 2001; 5: 394–400. https://doi.org/10.1016/s1364-6613(00)01707-1.
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