Hormonal and neuronal mechanisms of social attention and memory in the rhesus macaque (Macaca mulatta) Open Access
Solyst, James Andrew (2014)
Published
Abstract
Disorders impairing social behavior including autism and schizophrenia collectively affect over 2% of the population, and our limited understanding of the neurobiological mechanisms underlying these impairments has hindered the development of treatment strategies targeting these disorders. The goal of the present experiments was to advance our understanding of the neuronal and hormonal mechanisms mediating attention to and memory for social information. In doing so, we aimed to identify candidate mechanisms to be used in the development of optimal treatments for social impairments. To this end, the present experiments have examined in the rhesus macaque how neurons in the hippocampus encode faces into memory, and how social scenes are viewed under the influence of saline and oxytocin. We demonstrate that neurons in the macaque hippocampus discriminate both the social content and novelty of images through selective changes in firing rate for their preferred stimulus category. Using methods informed by screening tools for autism, we found that experience shifts exploration strategy, and that visual social cues drive the allocation of attention independent of the salience of low-level image features. Treatment with oxytocin amplifies this shift in exploration strategy and selectively increases attention towards social stimuli independent of low-level salience. Taken together, these data support previous work showing that the encoding of social information occurs within networks specific for social content and that the peptide oxytocin specifically regulates attention towards social information. Accordingly, our experiments have advanced our understanding of how social information is encoded in the brain and how social attention is regulated by exogenous oxytocin. These advances fill critical gaps in our knowledge of how social behavior is mediated through neurobiological mechanisms, and informs an ongoing movement towards optimizing treatment strategies for disorders impairing social function.
Table of Contents
Table of Contents
Chapter 1. Introduction.............................................................................................. 1
1.1 Alterations in attention to social stimuli in autism spectrum disorder.................................. 1
1.2 The importance of ecological relevance....................................................................................................... 6
1.3 Alterations in neural systems related to face-processing in autism spectrum disorders 10
1.4 Oxytocin and its effects on social behavior in primates.................................................................... 15
1.4.1 Oxytocin receptors and transmission....................................................................................................... 15
1.4.2 Intranasal administration of oxytocin................................................................................................... 18
1.4.3 Effects of oxytocin on anxiety........................................................................................................................ 19
1.4.3 Effects of oxytocin on attention to social stimuli............................................................................. 21
1.4.4 Effects of oxytocin on memory for social information................................................................... 22
1.4.5 Summary.................................................................................................................................................................... 23
1.5 Face processing by single neurons in the rhesus macaque................................................................ 24
1.5.1 Introduction............................................................................................................................................................ 24
1.5.2 Face-selective neurons in the macaque temporal lobe................................................................ 25
1.5.3 Encoding of faces by face-selective neurons........................................................................................ 26
1.5.4 Face-selectivity throughout the brain.................................................................................................... 29
1.5.5 Summary.................................................................................................................................................................... 31
Chapter 2. Face-selective neurons in the macaque hippocampus.................. 32
2.1 Abstract.............................................................................................................................................................................. 32
2.2 Introduction.................................................................................................................................................................... 32
2.3 Methods............................................................................................................................................................................... 34
2.3.1 Experimental Procedures................................................................................................................................. 34
2.3.2 Data Analysis........................................................................................................................................................... 37
2.4 Results.................................................................................................................................................................................. 41
2.4.1 Behavioral Results............................................................................................................................................... 41
2.4.2 Hippocampal Neurons Display Face-Selective Responses.......................................................... 44
2.4.3 Hippocampal Neurons Discriminate Image Category.................................................................. 46
2.4.4 Face-Selective Hippocampal Neurons Show Modulations in Firing Rate Related to Stimulus Novelty and Category 48
2.5 Discussion............................................................................................................................................................................ 49
Chapter 3. Social relevance drives viewing behavior independent of low-level salience in rhesus macaques 54
3.1 Abstract.............................................................................................................................................................................. 54
3.2 Introduction.................................................................................................................................................................... 55
3.3 Methods............................................................................................................................................................................... 60
3.3.1 Data Collection...................................................................................................................................................... 60
3.3.2 Scene Creation........................................................................................................................................................ 64
3.3.3 Data Analysis........................................................................................................................................................... 65
3.2 Results.................................................................................................................................................................................. 68
3.2.1 Viewing strategy changes with experience........................................................................................... 68
3.3.2 Scene contents are remembered across experience......................................................................... 71
3.3.3 Saliency does not account for social viewing preference............................................................. 71
3.3.4 Social relevance drives viewing behavior.............................................................................................. 77
3.4 Discussion............................................................................................................................................................................ 81
Chapter 4. Oxytocin increases attention selectively to social stimuli independent of low-level salience 86
4.1 Abstract.............................................................................................................................................................................. 86
4.2 Introduction.................................................................................................................................................................... 87
4.3 Methods............................................................................................................................................................................... 91
4.3.1 Data Collection...................................................................................................................................................... 91
4.3.2 Data Analysis........................................................................................................................................................... 93
4.4 Results.................................................................................................................................................................................. 96
4.4.1 Oxytocin alters viewing strategy................................................................................................................. 96
4.4.2 Oxytocin does not alter memory for manipulated items.......................................................... 100
4.4.3 Oxytocin increases time spent viewing monkeys............................................................................ 100
4.4.4 Oxytocin does not affect the number of items viewed................................................................. 102
4.4.5 Time-course of the effects of oxytocin on viewing behavior................................................... 103
4.4.6 Oxytocin affects the duration of the first fixation to faces....................................................... 105
4.4.7 Oxytocin alters social interest in specific characteristics......................................................... 108
4.4.8 Oxytocin does not alter viewing of low-level salience................................................................ 109
4.5 Discussion......................................................................................................................................................................... 114
Chapter 5. Discussion............................................................................................... 118
5.1 Interpretation............................................................................................................................................................ 118
5.1.1 Face-selective neurons in the macaque hippocampus.............................................................. 118
5.1.2 Social relevance drives the allocation of attention independent of low-level salience 119
5.1.3 Oxytocin increases attention selectively to social stimuli independent of low-level salience 121
5.2 Open questions and future directions......................................................................................................... 123
5.2.1 Social salience, social anxiety, or both?............................................................................................... 123
5.2.2 Interaction between endogenous and exogenous oxytocin and individual differences.................. 124
5.2.3 Manipulating social content with static scenes............................................................................. 125
5.2.4 Developing controlled tasks with high ecological relevance................................................. 126
5.3 Summary of findings................................................................................................................................................. 129
Appendix 1.................................................................................................................... 130
References................................................................................................................... 142
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