Landi SM, Viswanathan P, Serene S, Freiwald WA.
A fast link between face perception and memory in the temporal pole.
Science. 2021 Jul 30;373(6554):581-585. Epub 2021 Jul 1
PubMed.
In this interesting paper, Landi et al. provide a series of detailed investigations of macaque temporal pole and inferotemporal cell responses to faces and other stimuli. Despite cross-species differences, these findings might increase our understanding of face-recognition difficulties arising in human neurodegenerative diseases like the right-temporal variant of frontotemporal dementia (FTD) (Erkoyun et al., 2020) and posterior cortical atrophy (PCA, aka “visual-spatial Alzheimer’s disease”) (Graff-Radford et al., 2021).
The authors measured selectivity of macaque cell responses in right temporal pole and inferotemporal regions to both familiar and unfamiliar face, body, and object stimuli. Both temporal pole and inferotemporal cells responded selectively to face stimuli. However, while temporal pole cells responded more than three times more for familiar than unfamiliar monkey faces, there was no evidence of an effect of familiarity on inferotemporal cortex cell responses. Very high selectivity of temporal pole cells for familiar monkey faces was contrasted by similar inferotemporal responses for both monkey and human faces. Intriguingly, population response latencies were similar between temporal pole and inferotemporal cells. Given the lack of documented direct connections between temporal pole and inferotemporal regions in macaques, the authors propose the existence of two parallel pathways of face and person memory: one from inferotemporal to perirhinal and medial temporal regions, and another allowing rapid direct access to long-term semantic face information subserved by the temporal pole.
In the context of human neurodegenerative conditions, we see the following implications:
1. Apperceptive prosopagnosia (i.e., the inability to perceive and cognitively process the face) is a core feature of PCA and may be a defining feature of a proportion of individuals with ventral, visuoperceptual-predominant, PCA presentations (Crutch et al., 2017; Graff-Radford et al., 2021). Consistent with the apperceptive nature of face-perception difficulties, a ventral-clinico-radiological profile in PCA tends to comprise occipital and infero-temporoparietal rather than anterior-temporal atrophy (Groot et al., 2020). Whether the two proposed parallel pathways exist in humans raises the possibility of multiple routes to familiar-face recognition in PCA, with the hypothetical direct pathway proposed by Landi et al. possibly being relatively spared. However, it is worth noting that prominent low-level visual dysfunction arising in PCA may limit object identification regardless of stimulus type or category (Yong et al., 2014).
2. The authors suggest that their findings may relate to person-related agnosia following temporal-pole damage, carrying potential relevance to the right temporal variant of FTD. Documented radiological characteristics of right temporal variant include particular involvement of temporal poles extending to frontal and inferotemporal regions, emphasising right-sided predominant atrophy mirroring left-sided atrophy in semantic variant PPA (Erkoyun et al., 2020). Notably, initial prosopagnosia was more frequently observed in the right temporal variant of FTD (54 percent) versus semantic variant primary progressive aphasia (21 percent), behavioral variant FTD (4 percent) and typical (memory-predominant) Alzheimer’s disease (0 percent) (Abbate et al., 2019). It should be noted that although prosopagnosia at initial presentation is an uncommon feature of AD, it may arise in more advanced disease stages.
To conclude, we would like to reiterate that the current experiments were performed in macaques, hence detailed future investigation is essential to discover whether homologs of the proposed pathways also exist in human participants. Formal face-perception assessments are not routinely performed in a clinical/diagnostic setting, and these experiments are particularly challenging because both individuals with PCA or the right temporal variant of FTD have additional cognitive deficits (e.g., lower-level visual deficits in PCA) that may overlap with features of prosopagnosia. Furthermore, educational, cultural, and generational inter-individual differences may complicate the selection of appropriate stimuli (e.g., selecting famous or familiar faces). The ISTAART Atypical AD PIA is currently developing recommendations for assessing PCA features through a PCA working group, which will hopefully further facilitate the translation from basic neuroscience to clinical neuroscience studies.
References:
Ulugut Erkoyun H, Groot C, Heilbron R, Nelissen A, van Rossum J, Jutten R, Koene T, van der Flier WM, Wattjes MP, Scheltens P, Ossenkoppele R, Barkhof F, Pijnenburg Y.
A clinical-radiological framework of the right temporal variant of frontotemporal dementia.
Brain. 2020 Sep 1;143(9):2831-2843.
PubMed.
Graff-Radford J, Yong KX, Apostolova LG, Bouwman FH, Carrillo M, Dickerson BC, Rabinovici GD, Schott JM, Jones DT, Murray ME.
New insights into atypical Alzheimer's disease in the era of biomarkers.
Lancet Neurol. 2021 Mar;20(3):222-234.
PubMed.
Crutch SJ, Schott JM, Rabinovici GD, Murray M, Snowden JS, van der Flier WM, Dickerson BC, Vandenberghe R, Ahmed S, Bak TH, Boeve BF, Butler C, Cappa SF, Ceccaldi M, de Souza LC, Dubois B, Felician O, Galasko D, Graff-Radford J, Graff-Radford NR, Hof PR, Krolak-Salmon P, Lehmann M, Magnin E, Mendez MF, Nestor PJ, Onyike CU, Pelak VS, Pijnenburg Y, Primativo S, Rossor MN, Ryan NS, Scheltens P, Shakespeare TJ, Suárez González A, Tang-Wai DF, Yong KX, Carrillo M, Fox NC, Alzheimer's Association ISTAART Atypical Alzheimer's Disease and Associated Syndromes Professional Interest Area.
Consensus classification of posterior cortical atrophy.
Alzheimers Dement. 2017 Aug;13(8):870-884. Epub 2017 Mar 2
PubMed.
Groot C, Yeo BT, Vogel JW, Zhang X, Sun N, Mormino EC, Pijnenburg YA, Miller BL, Rosen HJ, La Joie R, Barkhof F, Scheltens P, van der Flier WM, Rabinovici GD, Ossenkoppele R.
Latent atrophy factors related to phenotypical variants of posterior cortical atrophy.
Neurology. 2020 Sep 22;95(12):e1672-e1685. Epub 2020 Jul 16
PubMed.
Yong KX, Shakespeare TJ, Cash D, Henley SM, Nicholas JM, Ridgway GR, Golden HL, Warrington EK, Carton AM, Kaski D, Schott JM, Warren JD, Crutch SJ.
Prominent effects and neural correlates of visual crowding in a neurodegenerative disease population.
Brain. 2014 Dec;137(Pt 12):3284-99. Epub 2014 Oct 27
PubMed.
Abbate C, Trimarchi PD, Inglese S, Damanti S, Dolci GA, Ciccone S, Rossi PD, Mari D, Arosio B, Bagarolo R, Giunco F, Cesari M.
Does the Right Focal Variant of Alzheimer's Disease Really Exist? A Literature Analysis.
J Alzheimers Dis. 2019;71(2):405-420.
PubMed.
Comments
University College London
VU University Medical Center
In this interesting paper, Landi et al. provide a series of detailed investigations of macaque temporal pole and inferotemporal cell responses to faces and other stimuli. Despite cross-species differences, these findings might increase our understanding of face-recognition difficulties arising in human neurodegenerative diseases like the right-temporal variant of frontotemporal dementia (FTD) (Erkoyun et al., 2020) and posterior cortical atrophy (PCA, aka “visual-spatial Alzheimer’s disease”) (Graff-Radford et al., 2021).
The authors measured selectivity of macaque cell responses in right temporal pole and inferotemporal regions to both familiar and unfamiliar face, body, and object stimuli. Both temporal pole and inferotemporal cells responded selectively to face stimuli. However, while temporal pole cells responded more than three times more for familiar than unfamiliar monkey faces, there was no evidence of an effect of familiarity on inferotemporal cortex cell responses. Very high selectivity of temporal pole cells for familiar monkey faces was contrasted by similar inferotemporal responses for both monkey and human faces. Intriguingly, population response latencies were similar between temporal pole and inferotemporal cells. Given the lack of documented direct connections between temporal pole and inferotemporal regions in macaques, the authors propose the existence of two parallel pathways of face and person memory: one from inferotemporal to perirhinal and medial temporal regions, and another allowing rapid direct access to long-term semantic face information subserved by the temporal pole.
In the context of human neurodegenerative conditions, we see the following implications:
1. Apperceptive prosopagnosia (i.e., the inability to perceive and cognitively process the face) is a core feature of PCA and may be a defining feature of a proportion of individuals with ventral, visuoperceptual-predominant, PCA presentations (Crutch et al., 2017; Graff-Radford et al., 2021). Consistent with the apperceptive nature of face-perception difficulties, a ventral-clinico-radiological profile in PCA tends to comprise occipital and infero-temporoparietal rather than anterior-temporal atrophy (Groot et al., 2020). Whether the two proposed parallel pathways exist in humans raises the possibility of multiple routes to familiar-face recognition in PCA, with the hypothetical direct pathway proposed by Landi et al. possibly being relatively spared. However, it is worth noting that prominent low-level visual dysfunction arising in PCA may limit object identification regardless of stimulus type or category (Yong et al., 2014).
2. The authors suggest that their findings may relate to person-related agnosia following temporal-pole damage, carrying potential relevance to the right temporal variant of FTD. Documented radiological characteristics of right temporal variant include particular involvement of temporal poles extending to frontal and inferotemporal regions, emphasising right-sided predominant atrophy mirroring left-sided atrophy in semantic variant PPA (Erkoyun et al., 2020). Notably, initial prosopagnosia was more frequently observed in the right temporal variant of FTD (54 percent) versus semantic variant primary progressive aphasia (21 percent), behavioral variant FTD (4 percent) and typical (memory-predominant) Alzheimer’s disease (0 percent) (Abbate et al., 2019). It should be noted that although prosopagnosia at initial presentation is an uncommon feature of AD, it may arise in more advanced disease stages.
To conclude, we would like to reiterate that the current experiments were performed in macaques, hence detailed future investigation is essential to discover whether homologs of the proposed pathways also exist in human participants. Formal face-perception assessments are not routinely performed in a clinical/diagnostic setting, and these experiments are particularly challenging because both individuals with PCA or the right temporal variant of FTD have additional cognitive deficits (e.g., lower-level visual deficits in PCA) that may overlap with features of prosopagnosia. Furthermore, educational, cultural, and generational inter-individual differences may complicate the selection of appropriate stimuli (e.g., selecting famous or familiar faces). The ISTAART Atypical AD PIA is currently developing recommendations for assessing PCA features through a PCA working group, which will hopefully further facilitate the translation from basic neuroscience to clinical neuroscience studies.
References:
Ulugut Erkoyun H, Groot C, Heilbron R, Nelissen A, van Rossum J, Jutten R, Koene T, van der Flier WM, Wattjes MP, Scheltens P, Ossenkoppele R, Barkhof F, Pijnenburg Y. A clinical-radiological framework of the right temporal variant of frontotemporal dementia. Brain. 2020 Sep 1;143(9):2831-2843. PubMed.
Graff-Radford J, Yong KX, Apostolova LG, Bouwman FH, Carrillo M, Dickerson BC, Rabinovici GD, Schott JM, Jones DT, Murray ME. New insights into atypical Alzheimer's disease in the era of biomarkers. Lancet Neurol. 2021 Mar;20(3):222-234. PubMed.
Crutch SJ, Schott JM, Rabinovici GD, Murray M, Snowden JS, van der Flier WM, Dickerson BC, Vandenberghe R, Ahmed S, Bak TH, Boeve BF, Butler C, Cappa SF, Ceccaldi M, de Souza LC, Dubois B, Felician O, Galasko D, Graff-Radford J, Graff-Radford NR, Hof PR, Krolak-Salmon P, Lehmann M, Magnin E, Mendez MF, Nestor PJ, Onyike CU, Pelak VS, Pijnenburg Y, Primativo S, Rossor MN, Ryan NS, Scheltens P, Shakespeare TJ, Suárez González A, Tang-Wai DF, Yong KX, Carrillo M, Fox NC, Alzheimer's Association ISTAART Atypical Alzheimer's Disease and Associated Syndromes Professional Interest Area. Consensus classification of posterior cortical atrophy. Alzheimers Dement. 2017 Aug;13(8):870-884. Epub 2017 Mar 2 PubMed.
Groot C, Yeo BT, Vogel JW, Zhang X, Sun N, Mormino EC, Pijnenburg YA, Miller BL, Rosen HJ, La Joie R, Barkhof F, Scheltens P, van der Flier WM, Rabinovici GD, Ossenkoppele R. Latent atrophy factors related to phenotypical variants of posterior cortical atrophy. Neurology. 2020 Sep 22;95(12):e1672-e1685. Epub 2020 Jul 16 PubMed.
Yong KX, Shakespeare TJ, Cash D, Henley SM, Nicholas JM, Ridgway GR, Golden HL, Warrington EK, Carton AM, Kaski D, Schott JM, Warren JD, Crutch SJ. Prominent effects and neural correlates of visual crowding in a neurodegenerative disease population. Brain. 2014 Dec;137(Pt 12):3284-99. Epub 2014 Oct 27 PubMed.
Abbate C, Trimarchi PD, Inglese S, Damanti S, Dolci GA, Ciccone S, Rossi PD, Mari D, Arosio B, Bagarolo R, Giunco F, Cesari M. Does the Right Focal Variant of Alzheimer's Disease Really Exist? A Literature Analysis. J Alzheimers Dis. 2019;71(2):405-420. PubMed.
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