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From inter-brain connectivity to inter-personal psychiatry
World Psychiatry ( IF 73.3 ) Pub Date : 2022-05-07 , DOI: 10.1002/wps.20987
Guillaume Dumas 1
Affiliation  

When it comes to symptom emergence and treatment of disorders, psychiatry and neuroscience do not always find common ground. On the one hand, neuroscientific research approaches mental disorders through their biological correlates using brain recordings; on the other, clinical psychiatry relies on self-report measures collected during face-to-face interviews. Taking into account both neural and experiential dimensions thus appears as one of the key challenges to the integration between neuroscience and psychiatry.

One aspect in which neuroscience and psychiatry do see eye to eye is in their restricted account of interpersonal dynamics. In psychiatry, the focus is primarily put on the mental state examination of the patient, although most mental disorders severely affect and are affected by social dynamics. Similarly, in neuroscience, the “social brain” has been paradoxically studied in isolated contexts, inferring that mere passive social perception and active social interaction are encoded in the same way at the brain level. Yet, research has widely shown that the development of children’s social abilities requires subtle social interactions with their parents, involving an active and reciprocal co-regulation of the exchanges. Recent advancements in social neuroscience suggest that the relationship between brains and social dynamics might offer a unique opportunity for the neuroscience-psychiatry integration while acknowledging the inherent socialness of mental disorders.

In 2002, a groundbreaking functional magnetic resonance imaging (fMRI) study introduced a technique called hyperscanning1, where the authors simultaneously scanned the brains of several participants while they were interacting through an economic game. This study paved the way for the design of realistic experimental protocols capable of capturing the crucial features of sociality, i.e. dynamicity and reciprocity, to investigate the neu­ral mechanisms supporting social cognition and behavior.

The idea quickly spread to other brain recording techniques, such as electroencephalography (EEG) and functional near-infrared spectroscopy (fNIRS), which are cheaper and more flexible for social tasks requiring direct face-to-face interaction. This led to the discovery of specific neural circuits that support social interaction and that differ from those enabling the sole perception of social stimuli. For instance, both mirror and mentalizing networks are simultaneously engaged, with a subtle modulation of shared representations and the maintenance of a distinction between self and other.

Beyond this better understanding at the intra-brain level, the development of hyperscanning has also inspired several teams of researchers to look at the inter-brain level, i.e. between-par­ticipants brain activity. The underlying hypothesis was that ­communication of information across brains might follow the same principles that govern communication of information in­side brains. Thus, it was expected to find coherent activity between one region and another, but extended to two or more individuals. This novel inter-personal and dynamic perspective on social cognition was strongly associated with the development of 4E cognition, arguing that the mind is not solely in the head, but is also embodied, embedded, enacted, and extended.

Thanks to hyperscanning recordings, a new type of neural correlate was identified: inter-brain connectivity (IBC)2. This can be defined as the synchronized brain activity of two or more people involved in a social scenario that can be attributed to their interaction rather than a shared external environment. All common neuroimaging techniques can be used to reveal IBC, from fMRI and fNIRS, which allow measuring amplitude correlation (i.e., when the brains activate regions at the same time), to EEG and magnetoencephalography, that provide sufficient temporal resolution to observe phase synchronization (i.e., when the brains present coherent oscillatory activity in time).

In the last two decades, the observation of IBC has grown from a few isolated studies to a whole new field now covering non-ver­bal and verbal exchanges, in dyadic and group contexts, with in­teraction between mother-infants, romantic couples, friends, but also complete strangers. Those experiments have identified many correlates of IBC, from behavioral synchronization and imitation of movement to language familiarity, empathic connection, and even human attachment. This massive growth has recently allowed the first meta-analyses and triggered the development of standardized IBC tools, consolidating both scientific progress and replicability in the nascent multi-brain neuroscience research.

But, how can psychiatry use this new form of multi-brain mea­surements? What can IBC bring to the understanding of psychiatric conditions, and how can it ultimately help in the daily practice of clinicians?

First, IBC can provide a neural correlate for core clinical features of mental disorders. For instance, the alteration of interactive social cognition may be more specific than that of perceptual social cognition3. In autism spectrum disorder, as an example, patients rarely mention misunderstanding of complex social plots in movies; they rather complain about their difficulties with improvising in real-time social interaction during daily life. Hyperscanning recordings can thus help in further exploring the mechanisms and manifestations of psychiatric conditions with a strong social dimension4.

Second, IBC can provide an objective measurement of the empathic connection or other social phenomena that are fundamental to the psychotherapeutic process but remain hard to capture at the biological level. For instance, hyperscanning studies have started to uncover the biological correlates of complex inter-personal phenomena such as the analgesic effect of affective touch5 or the therapeutic alliance6. In both cases, the alignment at affective and cognitive levels is reflected in the alignment at the neurobehavioral level.

So, IBC promises to better capture the underlying biological factors impacting psychiatric manifestations and treatment, without necessarily reducing them to only intra-personal processes.

Beyond these recent developments, we can also wonder what are the next steps for multi-brain neuroscience, and especially what potential avenues it can open for psychiatric research and clinical practice.

First, while early work was done in humans, the recent increased interest in IBC comes from multiple papers published with animal models7. Not only have these studies replicated the early observation of inter-brain correlates in humans, but they have also uncovered for the first time cellular mechanisms. This move from mesoscopic to microscopic levels opens possibilities to decipher which biological mechanisms can be targeted pharmacologically to potentially enhance IBC and with them neurobehavioral inter-personal dynamics.

Second, another recent trend is the move from multi-brain re­cording to multi-brain stimulations. The burgeoning field of hyper-stimulation8 may thus represent the next technological step to go from inter-brain correlational measurement to direct causal manipulation. Preliminary results already demonstrate that induction of inter-brain synchronization of neural processes shapes social interaction within groups of mice, and facilitates motor coordination in humans. If multi-brain electromagnetic stimulation provides insights about the causal factors modulating IBC and eventually sheds light onto biological mechanisms, a long-term challenge will be to move even beyond the traditional “correlation vs. causation” debate and provide an integrative explanation of the IBC phenomenon9. Ultimately, inter-personal neuromodulation through pharmacological compounds, electromagnetic stimulations, and even both, could open the way to new forms of therapeutics in psychiatry.

We have seen how the nascent multi-brain neuroscience may lead to transformative applications in psychiatry, from inter-brain measures for clinical characterization to inter-brain neuromodulation for treatments. Interestingly, this inter-personal psychiatry will also help take seriously our biological grounding as much as our social embedding.



中文翻译:

从大脑间连接到人际精神病学

在症状出现和疾病治疗方面,精神病学和神经科学并不总能找到共同点。一方面,神经科学研究通过使用大脑记录的生物学相关性来研究精神障碍;另一方面,临床精神病学依赖于面对面访谈期间收集的自我报告措施。因此,同时考虑神经和经验维度似乎是神经科学和精神病学之间整合的关键挑战之一。

神经科学和精神病学确实意见一致的一个方面是他们对人际动态的有限描述。在精神病学中,重点主要放在患者的精神状态检查上,尽管大多数精神障碍会严重影响社会动态并受其影响。同样,在神经科学中,“社会大脑”在孤立的环境中被自相矛盾地研究,推断仅仅是被动的社会感知和积极的社会互动在大脑水平上以相同的方式编码。然而,研究广泛表明,儿童社交能力的发展需要与父母进行微妙的社交互动,包括对交流进行积极和互惠的共同调节。

2002 年,一项突破性的功能磁共振成像 (fMRI) 研究引入了一种称为超扫描的技术1,作者在其中同时扫描了几个参与者的大脑,同时他们通过经济游戏进行互动。这项研究为设计能够捕捉社会性的关键特征(即动态性和互惠性)的现实实验协议铺平了道路,以研究支持社会认知和行为的神经机制。

这一想法很快传播到其他大脑记录技术,例如脑电图 (EEG) 和功能近红外光谱 (fNIRS),这些技术对于需要直接面对面互动的社交任务来说更便宜、更灵活。这导致发现了支持社交互动的特定神经回路,这些神经回路不同于那些能够单独感知社会刺激的神经回路。例如,镜像网络和心智化网络同时参与,对共享表征进行微妙的调制,并保持自我与他人之间的区别。

除了对脑内水平的更好理解之外,超扫描的发展还激发了几个研究小组研究大脑间水平,即参与者之间的大脑活动。潜在的假设是,跨大脑的信息交流可能遵循管理大脑内部信息交流的相同原则。因此,预计会在一个区域和另一个区域之间找到连贯的活动,但扩展到两个或更多个体。这种关于社会认知的新颖的人际和动态视角与 4E 认知的发展密切相关,认为心智不仅在头脑中,而且还体现、嵌入、制定和扩展。

由于超扫描记录,一种新型的神经相关被确定:脑间连接 (IBC) 2。这可以定义为参与社交场景的两个或更多人的同步大脑活动,这可以归因于他们的互动而不是共享的外部环境。所有常见的神经成像技术都可以用来揭示 IBC,从 fMRI 和 fNIRS,它们可以测量幅度相关性(即,当大脑同时激活区域时),到 EEG 和脑磁图,它们提供足够的时间分辨率来观察相位同步。即,当大脑及时呈现一致的振荡活动时)。

在过去的二十年里,对 IBC 的观察已经从一些孤立的研究发展到一个全新的领域,现在涵盖了非语言和语言交流,在二元和群体背景下,母婴、浪漫情侣、朋友之间的互动,但也完全陌生。这些实验已经确定了 IBC 的许多相关因素,从行为同步和运动模仿到语言熟悉度、移情联系,甚至是人类依恋。这种巨大的增长最近促成了第一次荟萃分析,并引发了标准化 IBC 工具的开发,巩固了新兴多脑神经科学研究的科学进步和可复制性。

但是,精神病学如何使用这种新形式的多脑测量?IBC 可以为了解精神疾病带来什么,以及它最终如何帮助临床医生的日常实践?

首先,IBC 可以为精神障碍的核心临床特征提供神经关联。例如,互动社会认知的改变可能比感性社会认知的改变更具体3。以自闭症谱系障碍为例,患者很少提及对电影中复杂的社会情节的误解;他们宁愿抱怨在日常生活中即兴进行实时社交互动时遇到的困难。因此,超扫描记录可以帮助进一步探索具有强烈社会维度4的精神疾病的机制和表现。

其次,IBC 可以提供对移情联系或其他社会现象的客观测量,这些现象对心理治疗过程至关重要,但在生物学水平上仍然难以捕捉。例如,超扫描研究已经开始揭示复杂的人际关系现象的生物学相关性,例如情感触摸5或治疗联盟6的镇痛作用。在这两种情况下,情感和认知水平的一致性反映在神经行为水平的一致性中。

因此,IBC 承诺更好地捕捉影响精神表现和治疗的潜在生物学因素,而不必将它们简化为仅个人内部过程。

除了这些最近的发展,我们还想知道多脑神经科学的下一步是什么,特别是它可以为精神病学研究和临床实践开辟哪些潜在途径。

首先,虽然早期的工作是在人类身上完成的,但最近对 IBC 的兴趣增加来自于用动物模型7发表的多篇论文。这些研究不仅复制了人类大脑间相关性的早期观察,而且还首次揭示了细胞机制。这种从介观到微观水平的转变为破译哪些生物学机制可以在药理学上靶向以潜在地增强 IBC 以及神经行为人际关系动力学提供了可能性。

其次,最近的另一个趋势是从多脑记录转向多脑刺激。因此,超刺激的新兴领域8可能代表下一个技术步骤,即从大脑间相关性测量到直接因果操作。初步结果已经表明,神经过程的脑间同步的诱导塑造了小鼠群体内的社会互动,并促进了人类的运动协调。如果多脑电磁刺激提供有关调节 IBC 的因果因素的见解并最终阐明生物学机制,那么长期挑战将是超越传统的“相关性与因果关系”辩论并提供 IBC 的综合解释现象9. 最终,通过药理学化合物、电磁刺激,甚至两者兼而有之的人际神经调节,可以为精神病学新形式的治疗开辟道路。

我们已经看到新生的多脑神经科学如何可能导致精神病学中的变革性应用,从用于临床表征的脑间测量到用于治疗的脑间神经调节。有趣的是,这种人际关系精神病学也将有助于认真对待我们的生物学基础,就像我们的社会嵌入一样。

更新日期:2022-05-10
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