Drug and Alcohol Dependence 146 (2015) 103–106
Contents lists available at ScienceDirect
Drug and Alcohol Dependence journal homepage: www.elsevier.com/locate/drugalcdep
Short communication
Blunted striatal responses to favorite-food cues in smokers Ania M. Jastreboff a,1 , Rajita Sinha b,c,e,2 , Cheryl M. Lacadie d,3 , Iris M. Balodis b,4 , Robert Sherwin a,5 , Marc N. Potenza b,c,e,∗,6 a
Department of Internal Medicine, Division of Endocrinology, Yale University School of Medicine, New Haven, CT, USA Department of Psychiatry Yale University School of Medicine, New Haven, CT, USA Child Study Center, Yale University School of Medicine, New Haven, CT, USA d Department of Diagnostic Radiology, Yale University School of Medicine, New Haven, CT, USA e Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA b c
a r t i c l e
i n f o
Article history: Received 18 June 2014 Received in revised form 11 August 2014 Accepted 5 September 2014 Available online 18 September 2014 Keywords: Smoking BMI fMRI Food cues
a b s t r a c t Background: Although tobacco-smoking is associated with relatively leaner body mass and smoking cessation with weight gain, the brain mechanisms underlying these relationships are not well understood. Smokers compared to non-smokers have shown diminished neural responses to non-tobacco rewarding stimuli (e.g., monetary rewards), but brain responses to favorite-food cues have not been investigated relative to smoking status. We hypothesized that smokers would exhibit diminished neural responses compared to non-smokers in response to favorite-food cues in motivation-reward and emotion-regulating regions of the brain. Methods: Twenty-three smokers and 23 non-smokers matched based on body mass index (BMI), age, and gender listened to personalized favorite-food cue, stress, and neutral-relaxing audiotapes during fMRI. Results: During favorite-food cue exposure, smokers versus non-smokers exhibited diminished activations in the caudate, putamen, insula, and thalamus. Neural responses during stress and neutralrelaxing conditions were similar across groups. Subjective food-craving ratings were similar across groups. Conclusions: The relatively diminished neural responses to favorite-food cues in smokers may contribute to lower BMI. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction A major barrier to quitting smoking (Chiolero et al., 2008) involves cessation-related weight gain (Filozof et al., 2004) and smoking-related leanness (Albanes et al., 1987; Chiolero et al., 2008). Concerns of weight gain may undermine smoking-cessation efforts and promote relapse (Meyers et al., 1997; Clark et al., 2004). Foods and drugs of abuse, including nicotine, activate brain circuits involved in motivation, learning, and behavioral reinforcement (Di
∗ Correspondence to: Connecticut Mental Health Center, Room S-104, 34 Park Street, New Haven, CT 06519, USA. Tel.: +1 203 974 7356; fax: +1 203 974 7366. E-mail address: [email protected] (M.N. Potenza). 1 2 Church Street South, Suite 209, New Haven, CT 06519, USA. 2 2 Church Street South, Suite 209, New Haven, CT 06519, USA. 3 300 Cedar Street, New Haven, CT 06519, USA. 4 1 Church Street, 7th floor, New Haven, CT 06510, USA. 5 300 Cedar Street, New Haven, CT 06519, USA. 6 34 Park Street, Room S-104, New Haven, CT 06519, USA. http://dx.doi.org/10.1016/j.drugalcdep.2014.09.006 0376-8716/© 2014 Elsevier Ireland Ltd. All rights reserved.
Chiara, 2002; Volkow et al., 2008). Brain reward regions, such as the striatum, and increased dopaminergic transmission (Wang et al., 2001) therein are associated with exposure to palatable foods and food cues, with concomitant increases in food craving and eating motivations (Kelley et al., 2005; Small et al., 2001). Neural responses to food cues differ by body mass index (BMI; Martin et al., 2010; Stice et al., 2008; Stoeckel et al., 2008), with greater responsivity of brain-reward regions and subjective food craving associated with higher BMI (Pelchat et al., 2004; Simansky, 2005; Stice et al., 2008). Nicotine has been found to decrease appetite and neural differences between responses to food and control pictures in lean, never-smokers (Kroemer et al., 2013). Given these data, we tested the hypothesis that smoking status would be associated with differences in neural responses in reward-motivation regions independent of BMI. We used an established fMRI task involving guided-imagery procedures employing individually generated personalized scripts. Using this procedure, we previously observed in obese and lean individuals differences in neural responses to favorite-food cue (Jastreboff et al., 2013). Here,
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A.M. Jastreboff et al. / Drug and Alcohol Dependence 146 (2015) 103–106
we examined neural responses to favorite-food cues and stress in smokers and non-smokers of similar BMI. We hypothesized that smokers as compared to non-smokers would exhibit decreased neural response to favorite-food cues in corticostriatal-limbic regions. 2. Methods and materials 2.1. Subjects Men and women, between ages 19 and 50 years, who were current daily smokers (≥10 cigarettes/day) and non-smokers (never smokers), but otherwise healthy, were recruited from the community via advertisement. Smoking status was assessed by number of cigarettes/day, age at onset of smoking, years of smoking, carbon monoxide (CO) level, and Fagerstrom Test for Nicotine Dependence (FTND; Heatherton et al., 1991). Exclusion criteria included chronic medical conditions, psychiatric disorders (DSM-IV criteria), neurological injuries or illnesses, chronic medication use for medical problems or psychiatric disorders, IQ < 90, inability to read and write in English, pregnancy, and claustrophobia or metal in body incompatible with MRI. Mood ratings were assessed using the Center for Epidemiological StudiesDepression (CES-D) scale (Radloff, 1977). The study was approved by the Yale Human Investigation Committee. All subjects provided signed informed consent.
Table 1 Demographic data and metabolic parameters for smokers and non-smokers. CO, carbon monoxide; FTND, Fagerstrom test for nicotine dependence; CES-D, Center for Epidemiological Studies-Depression.
Demographics Age (years) Gender (Female) IQ BMI (kg/m2 ) Metabolic measures Glucosefasting (mg/dL) Insulinfasting (uU/mL) HOMA-IR Smoking measures Cigarettes per day FTND score CO levels Years smoked Age at onset of smoking Mood measure CES-D
p
Smokers(N = 23)
Non-smokers(N = 23)
Mean ± SD
Mean ± SD
26.7 ± 7.1 43% 112.1 ± 8.6 28.0 ± 4.6
27.4 ± 7.3 39% 112.6 ± 9.6 26.8 ± 5.1
NS NS NS NS
95.3 ± 11.5 16.2 ± 11.9 4.0 ± 4.0
93.5 ± 8.5 13.9 ± 5.0 3.2 ± 1.3
NS NS NS
9.4 ± 7.1 2.5 ± 2.0 12.5 ± 9.3 7.5 ± 9.0 18.2 ± 2.5
0 0 2.4 ± 1.0 0 0
– 0.001
Contents lists available at ScienceDirect
Drug and Alcohol Dependence journal homepage: www.elsevier.com/locate/drugalcdep
Short communication
Blunted striatal responses to favorite-food cues in smokers Ania M. Jastreboff a,1 , Rajita Sinha b,c,e,2 , Cheryl M. Lacadie d,3 , Iris M. Balodis b,4 , Robert Sherwin a,5 , Marc N. Potenza b,c,e,∗,6 a
Department of Internal Medicine, Division of Endocrinology, Yale University School of Medicine, New Haven, CT, USA Department of Psychiatry Yale University School of Medicine, New Haven, CT, USA Child Study Center, Yale University School of Medicine, New Haven, CT, USA d Department of Diagnostic Radiology, Yale University School of Medicine, New Haven, CT, USA e Department of Neurobiology, Yale University School of Medicine, New Haven, CT, USA b c
a r t i c l e
i n f o
Article history: Received 18 June 2014 Received in revised form 11 August 2014 Accepted 5 September 2014 Available online 18 September 2014 Keywords: Smoking BMI fMRI Food cues
a b s t r a c t Background: Although tobacco-smoking is associated with relatively leaner body mass and smoking cessation with weight gain, the brain mechanisms underlying these relationships are not well understood. Smokers compared to non-smokers have shown diminished neural responses to non-tobacco rewarding stimuli (e.g., monetary rewards), but brain responses to favorite-food cues have not been investigated relative to smoking status. We hypothesized that smokers would exhibit diminished neural responses compared to non-smokers in response to favorite-food cues in motivation-reward and emotion-regulating regions of the brain. Methods: Twenty-three smokers and 23 non-smokers matched based on body mass index (BMI), age, and gender listened to personalized favorite-food cue, stress, and neutral-relaxing audiotapes during fMRI. Results: During favorite-food cue exposure, smokers versus non-smokers exhibited diminished activations in the caudate, putamen, insula, and thalamus. Neural responses during stress and neutralrelaxing conditions were similar across groups. Subjective food-craving ratings were similar across groups. Conclusions: The relatively diminished neural responses to favorite-food cues in smokers may contribute to lower BMI. © 2014 Elsevier Ireland Ltd. All rights reserved.
1. Introduction A major barrier to quitting smoking (Chiolero et al., 2008) involves cessation-related weight gain (Filozof et al., 2004) and smoking-related leanness (Albanes et al., 1987; Chiolero et al., 2008). Concerns of weight gain may undermine smoking-cessation efforts and promote relapse (Meyers et al., 1997; Clark et al., 2004). Foods and drugs of abuse, including nicotine, activate brain circuits involved in motivation, learning, and behavioral reinforcement (Di
∗ Correspondence to: Connecticut Mental Health Center, Room S-104, 34 Park Street, New Haven, CT 06519, USA. Tel.: +1 203 974 7356; fax: +1 203 974 7366. E-mail address: [email protected] (M.N. Potenza). 1 2 Church Street South, Suite 209, New Haven, CT 06519, USA. 2 2 Church Street South, Suite 209, New Haven, CT 06519, USA. 3 300 Cedar Street, New Haven, CT 06519, USA. 4 1 Church Street, 7th floor, New Haven, CT 06510, USA. 5 300 Cedar Street, New Haven, CT 06519, USA. 6 34 Park Street, Room S-104, New Haven, CT 06519, USA. http://dx.doi.org/10.1016/j.drugalcdep.2014.09.006 0376-8716/© 2014 Elsevier Ireland Ltd. All rights reserved.
Chiara, 2002; Volkow et al., 2008). Brain reward regions, such as the striatum, and increased dopaminergic transmission (Wang et al., 2001) therein are associated with exposure to palatable foods and food cues, with concomitant increases in food craving and eating motivations (Kelley et al., 2005; Small et al., 2001). Neural responses to food cues differ by body mass index (BMI; Martin et al., 2010; Stice et al., 2008; Stoeckel et al., 2008), with greater responsivity of brain-reward regions and subjective food craving associated with higher BMI (Pelchat et al., 2004; Simansky, 2005; Stice et al., 2008). Nicotine has been found to decrease appetite and neural differences between responses to food and control pictures in lean, never-smokers (Kroemer et al., 2013). Given these data, we tested the hypothesis that smoking status would be associated with differences in neural responses in reward-motivation regions independent of BMI. We used an established fMRI task involving guided-imagery procedures employing individually generated personalized scripts. Using this procedure, we previously observed in obese and lean individuals differences in neural responses to favorite-food cue (Jastreboff et al., 2013). Here,
104
A.M. Jastreboff et al. / Drug and Alcohol Dependence 146 (2015) 103–106
we examined neural responses to favorite-food cues and stress in smokers and non-smokers of similar BMI. We hypothesized that smokers as compared to non-smokers would exhibit decreased neural response to favorite-food cues in corticostriatal-limbic regions. 2. Methods and materials 2.1. Subjects Men and women, between ages 19 and 50 years, who were current daily smokers (≥10 cigarettes/day) and non-smokers (never smokers), but otherwise healthy, were recruited from the community via advertisement. Smoking status was assessed by number of cigarettes/day, age at onset of smoking, years of smoking, carbon monoxide (CO) level, and Fagerstrom Test for Nicotine Dependence (FTND; Heatherton et al., 1991). Exclusion criteria included chronic medical conditions, psychiatric disorders (DSM-IV criteria), neurological injuries or illnesses, chronic medication use for medical problems or psychiatric disorders, IQ < 90, inability to read and write in English, pregnancy, and claustrophobia or metal in body incompatible with MRI. Mood ratings were assessed using the Center for Epidemiological StudiesDepression (CES-D) scale (Radloff, 1977). The study was approved by the Yale Human Investigation Committee. All subjects provided signed informed consent.
Table 1 Demographic data and metabolic parameters for smokers and non-smokers. CO, carbon monoxide; FTND, Fagerstrom test for nicotine dependence; CES-D, Center for Epidemiological Studies-Depression.
Demographics Age (years) Gender (Female) IQ BMI (kg/m2 ) Metabolic measures Glucosefasting (mg/dL) Insulinfasting (uU/mL) HOMA-IR Smoking measures Cigarettes per day FTND score CO levels Years smoked Age at onset of smoking Mood measure CES-D
p
Smokers(N = 23)
Non-smokers(N = 23)
Mean ± SD
Mean ± SD
26.7 ± 7.1 43% 112.1 ± 8.6 28.0 ± 4.6
27.4 ± 7.3 39% 112.6 ± 9.6 26.8 ± 5.1
NS NS NS NS
95.3 ± 11.5 16.2 ± 11.9 4.0 ± 4.0
93.5 ± 8.5 13.9 ± 5.0 3.2 ± 1.3
NS NS NS
9.4 ± 7.1 2.5 ± 2.0 12.5 ± 9.3 7.5 ± 9.0 18.2 ± 2.5
0 0 2.4 ± 1.0 0 0
– 0.001
