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Long-lasting aftereffect of a single prism adaptation: shifts in vision and proprioception are independent

Abstract

After a single adaptation session to prisms with gradually incremented shift magnitude, the prism adaptation aftereffect was measured by open loop mid-sagittal pointing (O) to a visual target without visual feedback. This aftereffect corresponded to the summation of the shift in proprioception, measured by straight ahead pointing without vision (S), and the visual straight ahead judgement (V), measured by verbal stopping of an LED moving from two opposite directions. However, the measurement of the aftereffects made over a period of 7 days revealed significantly different decay curves in V, O and S. Surprisingly the S shift was still present up to 7 days after the training, while V had returned to the original level by 2 h, which was the first measurement after subjects returned to a normal visual environment. O had returned to pre-test level after 1 day. After 3 days Wilkinson’s (J Exp Psychol 89:250–257, 1971) additive hypothesis (O=SV) no longer fit the data. Rather “O=Pl−V”, where Pl (Pr) is the shift in proprioception measured by passive lateral arm movements from left (right), fitted better during the whole 7 days of aftereffect in our study. Therefore, the aftereffect of our strong prism adaptation revealed, firstly, that classical open loop pointing consisted of aftereffect shifts equal to the summation of the shifts in the two passively measurable aftereffect components, vision (V) and proprioception (Pl), rather than with active straight ahead pointing (S). Secondly, the decay of the shift in visual perception and in passively measurable proprioception is independent. The former decays fast, and the latter decays slowly with two separate waves. Thirdly, we suggest that the use of visual perception-dependent spatial codes for visual-manual transformation and the vision-independent internal egocentric reference frame are mutually exclusive. We proposed a model to explain these possible mechanisms.

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Abbreviations

CMl:

Neural network coding motor control and effecter response for movement from left,

CMr:

Neural network coding motor control and effecter response for movement from right,

CPl:

Neural network coding calibrated perceptual proprioception by movement from left,

CPr:

Neural network coding calibrated perceptual proprioception by movement from right,

CVa:

Neural network coding calibrated perceptual visual space,

IEREF:

Internal egocentric reference frame,

e-LTP :

Early long-term plasticity (including potentiation and depression),

l-LTP :

Late long-term plasticity (including potentiation and depression),

O :

Open loop pointing test,

Pl:

Passive proprioceptive straight ahead test from left arm movement,

Pr:

Passive proprioceptive straight ahead test from right arm movement,

S :

Straight ahead pointing test,

Va :

Visual straight ahead test averaged from the two directions of LED movement,

Vl:

Visual straight ahead test from left LED movement,

Vr:

Visual straight ahead test from right LED movement,

VMT:

Visuo-manual transformation.

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Correspondence to Yohko Hatada.

Appendix

Appendix

Model to explain the neural network involved in prism adaptation using right arm

The neural network involved in the tasks of Pl, S and O test measurements are shown in Fig. 5a–d. In the pre-test, all the components are in the naïve state. CVa: visual perception, CP: perceptual proprioception, CM: motor command and execution, the three consist of peripheral system and calibrated decoding CNS for Va and P and motor control CNS for M. CPl is the functional neural network whose property can be measured by the task Pl. This codes the calibrated perceptual shift of Pl. Similarly CPr and CVa are the functional neural networks that code the calibrated perceptual shifts of Pr and Va. V0 indicates a given visual target during open loop pointing at the Cartesian mid-line of the subject. The long-dash double-dotted line indicates the borders between CNS and the peripheral system. Within the entire CNS box, there are direct/indirect connections between all components. The lines here illustrate only the primary direct connections for these tasks. The simple dashed line indicates external signal flow for visual feedback of current arm position during prism adaptation. The short-dash dotted line indicates periphery (arm). IEREF: internal egocentric reference frame. VMT: visuo-arm transformation. Thickness for box lines indicates magnitude of deviation from naïve state. Thick single lined box indicates spatially rightward deviated coding, thick double lined box indicates leftward deviation. Grey lines are not active. The upper switch indicates mutual exclusiveness of IEREF and VMT. The lower switch is switched between the (CMr-CPr) circuit and (CMl-CPl) circuit depending on the direction of sagittal pointing of out-/inward arm movements, respectively, during prism adaptation.

Fig. 5
figure5

A model to explain the neural network involved in prism adaptation and its aftereffect using the right arm

Figure 5a depicts conceptual model of the circuit involved in prism adaptation training during late stage. Most adaptation happens during outward arm movement which has visual feedback when the finger reaches the target position, while inward arm movement does not give adaptation input since there is no visual feedback. Therefore, the visual feedback indicated by the dotted line gives an adaptation pressure for mostly the arm movements using the CMl-CPl circuit. Thus adaptation effects are weighted and distributed within this circuit in the system: CVa-VMT-CMl-CPl. Figure 5b depicts the activity during Pl test measurement at 0 h. We suggest that this has proprioceptive perceptive signals in CNS as main cause of adaptation and involves a minor contribution from afferent proprioceptive signal from peripheral effectors. Figure 5c depicts the activity during S test measurement on 7th day. We suggest straight ahead pointing uses IEREF instead of VMT since there is no visual input. We suggested that the increase of the magnitude of shift in IEREF could occur through l-LTP transfer via indirect connections within CNS (fine dotted line) from the original coding shifts in components like CPl (see detailed possible mechanisms in Y. Hatada et al., submitted). Fig. 5d depicts the activity during O test measurement at 0 h. Open loop pointing relies on a given visual target (V0) which then is translated through VMT, into motor command (CMl), using afferent proprioceptive feedback and modified calibration in CPl during the pointing arm movement.

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Hatada, Y., Rossetti, Y. & Miall, R.C. Long-lasting aftereffect of a single prism adaptation: shifts in vision and proprioception are independent. Exp Brain Res 173, 415–424 (2006). https://doi.org/10.1007/s00221-006-0381-2

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Keywords

  • Visuo-motor
  • Visuo-sensory
  • Sensory-motor
  • Long-term plasticity
  • Internal representation