"Long before it's in the papers"
January 28, 2015


Brain region linked to sense of personal space

Aug. 30, 2009
Courtesy Caltech
and World Science staff

In a find­ing that may shed light on the brain mech­a­nisms in­volved in so­cial be­hav­ior, neu­ro­sci­en­tists say they have iden­ti­fied a brain struc­ture re­spon­si­ble for our sense of per­son­al space.

The finding, de­scribed in the Aug. 30 is­sue of the jour­nal Na­ture Neu­ro­sci­ence, could of­fer in­sight in­to au­tism and oth­er dis­or­ders where so­cial dis­tance is an is­sue.

Patient SM, a wom­an with com­plete bi­lat­er­al amyg­da­la le­sions, pre­ferred to stand close to the ex­per­i­ment­er. On av­er­age, con­trol par­tic­i­pants pre­ferred to stand near­ly twice as far away from the same ex­per­i­ment­er. Im­ages drawn to scale. (Cred­it: Na­ture Neu­ro­science/Dan Ken­ne­dy (Cal­tech))

The struc­ture, the amyg­dala—a pair of al­mond-shaped re­gions deep wi­thin each side of the brain—was pre­vi­ously known to pro­cess strong neg­a­tive emo­tions, such as an­ger and fear, and is con­sid­ered the seat of emo­tion in the brain. How­ev­er, it had nev­er been linked rig­or­ously to real-life hu­man so­cial in­ter­ac­tion. 

The researchers, led by neu­ro­sci­ent­ist Ralph Adolphs and post­doc­tor­al schol­ar Dan­iel P. Ken­ne­dy at the Cal­i­for­nia In­sti­tute of Tech­nol­o­gy, made the link with the help of a pa­tient, a 42-year-old wom­an known as SM to pro­tect her pri­va­cy. 

SM has ex­ten­sive dam­age to the amyg­da­la on both sides of her brain. This “gives us an op­por­tun­ity to study the role of the amyg­da­la in hu­mans,” said Ken­ne­dy, the lead au­thor of the new re­port.

SM has trou­ble rec­og­niz­ing fear in the faces of oth­ers, and in judg­ing the trust­wor­thi­ness of some­one, two con­se­quenc­es of amyg­da­la le­sions that Adolphs and col­leagues pub­lished in pri­or stud­ies.

Dur­ing his years of stu­dying her, Adolphs al­so no­ticed that the very out­go­ing SM is al­most too friend­ly, to the point of “vi­o­lat­ing” what oth­ers might per­ceive as their own per­son­al space. “She is ex­tremely friend­ly, and she wants to ap­proach peo­ple more than nor­mal. It’s some­thing that im­me­di­ately be­comes ap­par­ent as you in­ter­act with her,” said Ken­ne­dy.

Pre­vi­ous stud­ies of hu­mans nev­er had re­vealed an as­socia­t­ion be­tween the amyg­da­la and per­son­al space. From their knowl­edge of the lit­er­a­ture, how­ev­er, the re­search­ers knew that mon­keys with amyg­da­la le­sions pre­ferred to stay in clos­er proxim­ity to oth­er mon­keys and hu­mans than did healthy mon­keys. 

Adolphs, Ken­ne­dy, and col­leagues de­vised an ex­pe­ri­ment to measure and com­pare SM’s sense of per­son­al space with that of healthy vol­un­teers. The test sub­ject stands a set dis­tance from an ex­pe­ri­menter, then walks to­ward the ex­pe­ri­menter and stops at the point where they feel most com­fort­a­ble. The chin-to-chin dis­tance be­tween the sub­ject and the ex­pe­ri­menter is then meas­ured us­ing a la­ser.

Among the 20 oth­er sub­jects, the av­er­age pre­ferred dis­tance was 64 cen­time­ter­s—roughly two feet. SM’s pre­ferred dis­tance was just 34 cen­time­ters, or about one foot. Un­like oth­er sub­jects, who re­ported feel­ings of dis­com­fort when the ex­pe­ri­menter went clos­er than their pre­ferred dis­tance, there was no point at which SM be­came un­com­fort­a­ble; even nose-to-nose, she was at ease. Fur­ther­more, her pre­ferred dis­tance did­n’t change based on who the ex­pe­ri­menter was and how well she knew them. 

“Re­spect­ing some­one’s space is a crit­i­cal as­pect of hu­man so­cial in­ter­ac­tion, and some­thing we do au­to­mat­ic­ally and ef­fort­less­ly,” Ken­ne­dy said. “These find­ings sug­gest that the amyg­da­la, be­cause it is nec­es­sary for the strong feel­ings of dis­com­fort that help to re­pel peo­ple from one anoth­er, plays a cen­tral role in this pro­cess. They al­so help to ex­pand our un­der­stand­ing of the role of the amyg­da­la in real-world so­cial in­ter­ac­tions.”

Adolphs and col­leagues then used brain scans to ex­am­ine the ac­tiva­t­ion of the amyg­da­la in a sep­a­rate group of healthy sub­jects who were told when an ex­pe­ri­menter was ei­ther in close proxim­ity or far away from them. When in the scan­ner, sub­jects could not see, feel, or hear the ex­pe­ri­menter; nev­ertheless, their amyg­da­lae lit up when they be­lieved the ex­pe­ri­menter to be close by. No ac­ti­vity was de­tected when sub­jects thought the ex­pe­ri­menter was on the oth­er side of the room.

“It was just the idea of anoth­er per­son be­ing there, or not, that trig­gered the amyg­da­la,” Ken­ne­dy said. The re­search­ers be­lieve that interper­son­al dis­tance is not some­thing we con­sciously think about, al­though, un­like SM, we be­come acutely aware when our space is vi­o­lat­ed. Ken­ne­dy re­counts his own ex­perience with hav­ing his per­son­al space vi­o­lat­ed dur­ing a wed­ding: “I felt really un­com­fort­a­ble, and al­most fell over a chair while back­ing up to get some space.”

Across cul­tures, ac­cept­ed interper­son­al dis­tances can vary dra­mat­ic­ally. Peo­ple who live in cul­tures where space is at a pre­mi­um, say, Chi­na or Ja­pan, seem­ingly tol­er­ant of much clos­er dis­tances than in­di­vid­u­als in, say, the Un­ited States. And our pre­ferred per­son­al dis­tance can vary de­pend­ing on our situa­t­ion, mak­ing us far more will­ing to ac­cept less space in a crowd­ed sub­way car than we would be at the of­fice.

One ex­plana­t­ion for this varia­t­ion, Ken­ne­dy said, is that cul­tur­al pref­er­ences and ex­periences af­fect the brain over time and how it re­sponds in par­tic­u­lar situa­t­ions. “If you’re in a cul­ture where stand­ing close to some­one is the norm, you’d learn that was ac­ceptable and your per­son­al space would vary ac­cord­ing­ly,” he said. “Even then, if you vi­o­late the ac­cept­ed cul­tur­al dis­tance, it will make peo­ple un­com­fort­a­ble, and the amyg­da­la will drive that feel­ing.”

The find­ings may have rel­e­vance to stud­ies of au­tism, a com­plex dis­or­der that af­fects an in­di­vid­u­al’s abil­ity to in­ter­act so­cially and com­mu­ni­cate with oth­ers. “We are really in­ter­est­ed in look­ing at per­son­al space in peo­ple with au­tism, es­pe­cially giv­en find­ings of amyg­da­la dys­func­tion in au­tism. We know that some peo­ple with au­tism do have prob­lems with per­son­al space and have to be taught what it is and why it’s im­por­tan­t,” Ken­ne­dy said. 

He al­so adds a word of cau­tion: “It’s clear that amyg­da­la dys­func­tion can­not ac­count for all the so­cial im­pair­ments in au­tism, but likely con­tri­butes to some of them and is def­i­nitely some­thing that needs to be stud­ied fur­ther.”

* * *

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In a finding that may shed light on the brain mechanisms involved in social behavior, neuroscientists at the California Institute of Technology have identified a brain structure responsible for our sense of personal space. The discovery, described in the Aug/ 30 issue of the journal Nature Neuroscience, could offer insight into autism and other disorders where social distance is an issue. The structure, the amygdala—a pair of almond-shaped regions located in the medial temporal lobes—was previously known to process strong negative emotions, such as anger and fear, and is considered the seat of emotion in the brain. However, it had never been linked rigorously to real-life human social interaction. The scientists, led by neuroscientist Ralph Adolphs and postdoctoral scholar Daniel P. Kennedy at Caltech, made the link with the help of a patient, a 42-year-old woman known as SM to protect her privacy. SM has extensive damage to the amygdala on both sides of her brain. This “gives us an opportunity to study the role of the amygdala in humans,” said Kennedy, the lead author of the new report. SM has trouble recognizing fear in the faces of others, and in judging the trustworthiness of someone, two consequences of amygdala lesions that Adolphs and colleagues published in prior studies. During his years of studying her, Adolphs also noticed that the very outgoing SM is almost too friendly, to the point of “violating” what others might perceive as their own personal space. “She is extremely friendly, and she wants to approach people more than normal. It’s something that immediately becomes apparent as you interact with her,” said Kennedy. Previous studies of humans never had revealed an association between the amygdala and personal space. From their knowledge of the literature, however, the researchers knew that monkeys with amygdala lesions preferred to stay in closer proximity to other monkeys and humans than did healthy monkeys. Adolphs, Kennedy, and colleagues devised an experiment to quantify and compare SM’s sense of personal space with that of healthy volunteers. The test subject stands a set distance from an experimenter, then walks toward the experimenter and stops at the point where they feel most comfortable. The chin-to-chin distance between the subject and the experimenter is then measured using a laser. Among the 20 other subjects, the average preferred distance was 64 centimeters—roughly two feet. SM’s preferred distance was just 34 centimeters, or about one foot. Unlike other subjects, who reported feelings of discomfort when the experimenter went closer than their preferred distance, there was no point at which SM became uncomfortable; even nose-to-nose, she was at ease. Furthermore, her preferred distance didn’t change based on who the experimenter was and how well she knew them. “Respecting someone’s space is a critical aspect of human social interaction, and something we do automatically and effortlessly,” Kennedy said. “These findings suggest that the amygdala, because it is necessary for the strong feelings of discomfort that help to repel people from one another, plays a central role in this process. They also help to expand our understanding of the role of the amygdala in real-world social interactions.” Adolphs and colleagues then used brain scans to examine the activation of the amygdala in a separate group of healthy subjects who were told when an experimenter was either in close proximity or far away from them. When in the scanner, subjects could not see, feel, or hear the experimenter; nevertheless, their amygdalae lit up when they believed the experimenter to be close by. No activity was detected when subjects thought the experimenter was on the other side of the room. “It was just the idea of another person being there, or not, that triggered the amygdala,” Kennedy said. The researchers believe that interpersonal distance is not something we consciously think about, although, unlike SM, we become acutely aware when our space is violated. Kennedy recounts his own experience with having his personal space violated during a wedding: “I felt really uncomfortable, and almost fell over a chair while backing up to get some space.” Across cultures, accepted interpersonal distances can vary dramatically. People who live in cultures where space is at a premium, say, China or Japan, seemingly tolerant of much closer distances than individuals in, say, the United States. And our preferred personal distance can vary depending on our situation, making us far more willing to accept less space in a crowded subway car than we would be at the office. One explanation for this variation, Kennedy said, is that cultural preferences and experiences affect the brain over time and how it responds in particular situations. “If you’re in a culture where standing close to someone is the norm, you’d learn that was acceptable and your personal space would vary accordingly,” he said. “Even then, if you violate the accepted cultural distance, it will make people uncomfortable, and the amygdala will drive that feeling.” The findings may have relevance to studies of autism, a complex neurodevelopmental disorder that affects an individual’s ability to interact socially and communicate with others. “We are really interested in looking at personal space in people with autism, especially given findings of amygdala dysfunction in autism. We know that some people with autism do have problems with personal space and have to be taught what it is and why it’s important,” Kennedy said. He also adds a word of caution: “It’s clear that amygdala dysfunction cannot account for all the social impairments in autism, but likely contributes to some of them and is definitely something that needs to be studied further.”